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Visual Processing of Faces in Temporal Cortex: Physiological Evidence for a Modular Organization and Possible Anatomical Correlates
Abstract
Physiological recordings along the length of the upper bank of the superior temporal sulcus (STS) revealed cells each of which was selectively responsive to a particular view of the head and body. Such cells were grouped in large patches 3-4 mm across. The patches were separated by regions of cortex containing cells responsive to other stimuli. The distribution of cells projecting from temporal cortex to the posterior regions of the inferior parietal lobe was studied with retrogradely transported fluorescent dyes. A strong temporoparietal projection was found originating from the upper bank of the STS. Cells projecting to the parietal cortex occurred in large patches or bands. The size and periodicity of modules defined through anatomical connections matched the functional subdivisions of the STS cortex involved in face processing evident in physiological recordings. It is speculated that the temporoparietal projections could provide a route through which temporal lobe analysis of facial signals about the direction of others' attention can be passed to parietal systems concerned with spatial awareness.
... In principle, there may be a systematic spatial organization to gazeselective neurons based on their spatial receptive fields, feature specificity (e.g. tuning to angles of gaze varying from left to right), or both-similar to the columnar organization of functionally related neurons described for simple visual features in the early visual cortex [48] and for more complex features in the temporal cortex [49,50]. Future work might explore the spatial organization of gaze-selective processing with the use of fMRI-adaptation and/or retinotopic mapping in humans, as well as single-cell recordings in non-human primates. ...
... The first two of these might be achieved in part by retinally specific representations of gaze direction, as revealed in the current study. While it is not yet clear how information about gaze direction is related to the position of other objects and events in the environment, this might rely on interactions between temporal and parietal mechanisms coding information about social attention and spatial position, respectively [9,50,51]. Future work might also profitably investigate the extension of the current paradigm to naturalistic environments, such as whether the form of spatial selectivity to adaptation observed in the present study persists in visual environments that contain richer cues to the spatial relations between objects and engage higher-level functions of gaze perception, such as joint attention. ...
A person's focus of attention is conveyed by the direction of their eyes and face, providing a simple visual cue fundamental to social interaction. A growing body of research examines the visual mechanisms that encode the direction of another person's gaze as we observe them. Here we investigate the spatial receptive field properties of these mechanisms, by testing the spatial selectivity of sensory adaptation to gaze direction. Human observers were adapted to faces with averted gaze presented in one visual hemifield, then tested in their perception of gaze direction for faces presented in the same or opposite hemifield. Adaptation caused strong, repulsive perceptual aftereffects, but only for faces presented in the same hemifield as the adapter. This occurred even though adapting and test stimuli were in the same external location across saccades. Hence, there was clear evidence for retinotopic adaptation and a relative lack of either spatiotopic or spatially invariant adaptation. These results indicate that adaptable representations of gaze direction in the human visual system have retinotopic spatial receptive fields. This strategy of coding others' direction of gaze with positional specificity relative to one's own eye position may facilitate key functions of gaze perception, such as socially cued shifts in visual attention.
... These findings suggest that the face-processing areas identified in the monkey STS and inferior temporal (IT) cortex most likely correspond to the human posterior STS and lateral fusiform gyrus (FFA), respectively. The Hoffman and Haxby (2000) scheme of the STS processing variable face aspects and the FFA processing invariant face aspects is likely to be a simplification because single-cell, anatomical and functional imaging all suggest an organization with several patches of cortex processing faces within the STS and IT of the monkey (Harries and Perrett, 1991; Tsao et al., 2006). ...
... Most neural models of social cognition see the STS as part of a core system dealing with social perception per se (cf Allison et al., 2000), and postulate that connections with the 'extended' system (including insula, orbitofrontal, cingulate , anterior temporal, somatosensory and parietal cortices and the amygdala) serve to extract meaning from social perceptions and control reactions (Haxby et al., 2000). For example, the ability to follow gaze, and, in cases where the other's attention is directed at a specific object, the ability to share attention with the observed agent, is likely to be underpinned by connections between the STS and the intraparietal sulcus (Harries and Perrett, 1991). The direction, or target, of another's attention is computed by neurons in the STS specifically responsive to eye-gaze direction, head orientation and bodily orientation (Perrett et al., 1985Perrett et al., , 1992), while the parietal cortex is involved in (covertly) directing the observer's spatial attention (cf. ...
This article reviews recent ideas about visual pathways and mechanisms in the brains of human and non-human primates that support social cognition. It shows how the detection of visual cues provides a basis for guiding the observer's behaviour in ways that are based on the current and likely future behaviour of others. These visual mechanisms underpin social cognition, but do not rely on understanding others' minds. They provide what one could call a 'mechanistic' description of others' behaviour and of social events in terms of constituent components of actions, their causes and consequences, and expected future occurrence. The article argues that the superior temporal sulcus forms the prime neural substrate for forming descriptions of the 'mechanics' of social events.
... Recognition learning is accomplished by i n teractions between inferotemporal cortex IT and hippocampal formation, among other brain areas Desimone, 1991;Desimone and Ungerleider, 1989;Eichenbaum, Otto, and Cohen, 1994;Gochin, Miller, Gross, and Gerstein, 1991;Harries and Perrett, 1991;Mishkin, 1978Mishkin, , 1982Mishkin and Appenzeller, 1987;Perrett, Mistlin, and Chitty, 1987;Schwartz, Desimone, Albright, and Gross, 1983;Squire and Zola-Morgan, 1991. These interactions include the matching process that modulates the course of recognition learning in IT cortex and the course of reinforcement learning in thalamocortico-amygdala circuits. ...
... Level F 2 properties may be compared with properties of cell activations in inferotemporal cortex IT during recognition learning in monkeys. The ability o f F 2 nodes to learn categories with di erent levels of generalization clari es how some IT cells can exhibit high speci city, such as selectivity to views of particular faces, while other cells respond to broader features of the animal's environment Desimone and Ungerleider, 1989;Gochin et al., 1991;Harries and Perrett, 1991;Mishkin, 1982;Mishkin and Appenzeller, 1987;Perrett, Mistlin, and Chitty, 1987;Schwartz et al., 1983;Seibert and Waxman, 1991. Moreover, when monkeys are exposed to easy and di cult discriminations Spitzer, Desimone, and Moran, 1988, in the di cult condition the animals adopted a stricter internal criterion for discriminating matching from nonmatching stimuli... the animals' internal representations of the stimuli were better separated, independent of the criterion used to discriminate them... increased e ort appears to cause enhancement of the responses and sharpened selectivity for attended stimuli" pp. ...
The concepts of declarative memory and procedural memory have been used to distinguish two basic types of learning. A neural network model suggests how such memory processes work together as recognition learning, reinforcement learning, and sensorimotor learning take place during adaptive behaviors. To coordinate these processes, the hippocampal formation and cerebellum each contains circuits that learn to adaptively time their outputs. Within the model, hippocampal timing helps to maintain attention on motivationally salient goal objects during variable task-related delays, and cerebellar timing controls the release of conditioned responses. This property is part of the model's description of how cognitive-emotional interactions focus attention on motivationally valued cues, and how this process breaks down due to hippocampal ablation. The model suggests that the hippocampal mechanisms that help to rapidly draw attention to salient cues could prematurely release motor commands were not the release of these commands adaptively timed by the cerebellum. The model hippocampal system modulates cortical recognition learning without actually encoding the representational information that the cortex encodes. These properties avoid the difficulties faced by several models that propose a direct hippocampal role in recognition learning. Learning within the model hippocampal system controls adaptive timing and spatial orientation. Model properties hereby clarify how hippocampal ablations cause amnesic symptoms and difficulties with tasks which combine task delays, novelty detection, and attention toward goal objects amid distractions. When these model recognition, reinforcement, sensorimotor, and timing processes work together, they suggest how the brain can accomplish conditioning of multiple sensory events to delayed rewards, as during serial compound conditioning.
... The explanations of amodal completion have heretofore emphasized amodal completion of BCS boundaries, as in Figures 26F and 30F. These completed boundaries are recognized via direct BCS -> ORS pathways, as in Figure 9, which are interpreted neurobiologically in terms of interactions between extrastriate visual cortex and temporal cortex, respectively (Desimone, 1991;Desimone, Schein, Moran, & Ungerleider, 1985;Desimone & Ungerleider, 1989;Cochin, Miller, Gross, & Gerstein, 1991;Harries & Perrett, 1991;Mishkin, 1978Mishkin, ,1982Mishkin & Appenzeller, 1987;Perrett, Mistlin, & Chitty, 1987;Schiller, 1994Schiller, , 1995Schwartz, Desimone, Albright, & Gross, 1983;Zeki, 1983aZeki, , 1983b. The amodally completed boundaries are perceptually invisible if only because BCS outputs are derived from a complex-cell pooling process that combines signals from opposite contrast polarities and all colors to define the strongest possible boundaries (Thorell, DeValois, & Albrecht, 1984). ...
This article develops the FACADE theory of 3-dimensional (3-D) vision and figure–ground separation to explain data concerning how 2-dimensional pictures give rise to 3-D percepts of occluding and occluded objects. The model describes how geometrical and contrastive properties of a picture can either cooperate or compete when forming the boundaries and surface representations that subserve conscious percepts. Spatially long-range cooperation and spatially short-range competition work together to separate the boundaries of occluding figures from their occluded neighbors. This boundary ownership process is sensitive to image T junctions at which occluded figures contact occluding figures. These boundaries control the filling-in of color within multiple depth-sensitive surface representations. Feedback between surface and boundary representations strengthens consistent boundaries while inhibiting inconsistent ones. Both the boundary and the surface representations of occluded objects may be amodally completed, while the surface representations of unoccluded objects become visible through modal completion. Functional roles for conscious modal and amodal representations in object recognition, spatial attention, and reaching behaviors are discussed. Model interactions are interpreted in terms of visual, temporal, and parietal cortices.
... The STS projects onto the parietal intraparietal cortex in macaques (Harries and Perrett, 1991). The lateral part of this structure (lateral parietal area, LIP) houses "gaze mirror neurons, " i.e., neurons that fire both, when looking at a specific location and when watching someone else gazing toward the same location (Shepherd et al., 2009). ...
Social gaze has received much attention in social cognition research in both human and non-human animals. Gaze following appears to be a central skill for acquiring social information, such as the location of food and predators, but can also draw attention to important social interactions, which in turn promotes the evolution of more complex socio-cognitive processes such as theory of mind and social learning. In the past decades, a large number of studies has been conducted in this field introducing differing methodologies. Thereby, various factors influencing the results of gaze following experiments have been identified. This review provides an overview of the advances in the study of gaze following, but also highlights some limitations within the research area. The majority of gaze following studies on animals have focused on primates and canids, which limits evolutionary interpretations to only a few and closely related evolutionary lineages. This review incorporates new insights gained from previously understudied taxa, such as fishes, reptiles, and birds, but it will also provide a brief outline of mammal studies. We propose that the foundations of gaze following emerged early in evolutionary history. Basic, reflexive co-orienting responses might have already evolved in fishes, which would explain the ubiquity of gaze following seen in the amniotes. More complex skills, such as geometrical gaze following and the ability to form social predictions based on gaze, seem to have evolved separately at least two times and appear to be correlated with growing complexity in brain anatomy such as increased numbers of brain neurons. However, more studies on different taxa in key phylogenetic positions are needed to better understand the evolutionary history of this fundamental socio-cognitive skill.
... One interesting observation of the studies using single-cell recordings was that face-selective cells in the superior temporal sulcus tended to occur in recurring 3-5 mm patches (Harries and Perrett, 1991). The extension of fMRI from human to monkey studies has replicated that observation and refined single-cell recordings by improving their targeting. ...
Face perception is a socially important but complex process with many stages and many facets. There is substantial evidence from many sources that it involves a large extent of the temporal lobe, from the ventral occipitotemporal cortex and superior temporal sulci to anterior temporal regions. While early human neuroimaging work suggested a core face network consisting of the occipital face area, fusiform face area, and posterior superior temporal sulcus, studies in both humans and monkeys show a system of face patches stretching from posterior to anterior in both the superior temporal sulcus and inferotemporal cortex. Sophisticated techniques such as fMRI adaptation have shown that these face-activated regions show responses that have many of the attributes of human face processing. Lesions of some of these regions in humans lead to variants of prosopagnosia, the inability to recognize the identity of a face. Lesion, imaging, and electrophysiologic data all suggest that there is a segregation between identity and expression processing, though some suggest this may be better characterized as a distinction between static and dynamic facial information.
... Macaques were used in early experiments, which discovered "face cells" within the temporal cortex -cells that responded to faces alone but not objects or other stimuli (Bruce, Desimone, & Gross, 1981;Gross, De Rocha-Miranda, & Bender, 1972). Cells responsive to faces in primates have been found across visual sub-regions of the temporal cortex, including the Superior Temporal Sulcus (STS) and lateral and ventral regions of inferior temporal (IT) cortex (Harries & Perrett, 1991;Perrett, Hietanen, Oram, & Benson, 1992;Perrett, Mistlin, & Chitty, 1987). ...
This thesis provides novel neuroimaging insights into the brain activity related to the processing of highly salient infant faces. Specifically, I provide new information about the spatial and temporal aspects of brain activity for processing infant faces within four experimental investigations. Overall, the presented findings provide novel, important insights into: (1) our current understanding of how the brain processes salient, infant faces, (2) human face perception more generally, and (3) potential implications for how we provide care to our young.
In Chapter 1, I review the literature on human face processing, and infant face processing. I draw together insights from prosopagnosia and single-cell studies in primates, moving on to discuss functional neuroimaging findings highlighting a dedicated spatial network of regions for face processing within the brain. The current evidence has good knowledge of ‘what’ and ‘where,’ but lacks a temporal dimension: ‘when.’ I then move on to discuss models of face perception, and how the dominant narrative involves a hierarchical, feedforward process, which is at odds with current knowledge about top-down interactions between brain regions. Lastly, I summarise our current understanding of human parental brain networks.
In Chapter 2, I present two quantitative meta-analyses of aggregated fMRI data, using activation likelihood estimation (ALE) analysis. First, I explore nulliparous women viewing infant faces, and second, I explore mothers viewing their own infants’ face. I present findings relating to the spatial coordinates of these two intriguing contrasts, including the apparent left lateralisation of infant face processing in motherhood. I reflect upon how the field of fMRI studies has thus far been limited in its ability to explain the temporal dimension of face processing (“when”) and set a precedent for a greater exploration of infant face processing using temporally sensitive brain imaging methodology and analytic methods.
In Chapter 3, I present the analysis of a dataset exploring how the human brain processes infant and adult faces, replicating previous findings of a privileged processing route when viewing infant faces to support sensitive and swift caregiving. I then advance the field by exploring how the human brain also processes juvenile and adult animal faces to test the hypothesis that the infant schema may operate in a cross-species fashion. I report evidence demonstrating that baby animals (kittens and puppies) also trigger an early orbitofrontal cortex response (120ms), that guides the brain to provide sensitive caregiving – “cuteness ignition”.
In Chapter 4, I analyse the same dataset as in Chapter 3, this time using a classifier (discriminant analysis) to pose the question as to how the adult brain categorises different kinds of faces. This chapter provides proof of principle for the ability of classification analysis to discover the spatiotemporal features needed to separate and predict up to six classes of face stimuli. The importance of the beta band and the time window of 60-180ms post stimulus presentation for face categorisation are both emphasised. The results provide further evidence for the importance of “when” components in brain activity within the human brain, especially when it comes to distinguishing between highly salient categories such as “cute” baby and baby animal faces. This method also provides exciting new avenues for research into the human parental brain and temporally sensitive parent-infant interactions.
Chapter 5 addresses how we can use more nuanced experimental paradigms in fMRI, combined with sensitive network analysis, to draw inferences about how the brain learns about characterological features of infant faces (emotionality). While previous chapters explored the short ‘when’ of infant face processing, this chapter addresses the long ‘when’ involving learning. I report upon a network involving orbitofrontal cortex, amygdala and hippocampus, which is more active for infant faces with a happier temperament and expression of emotionality. This has important implications for social learning, and perhaps for attachment and empathy.
Lastly, in Chapter 6 I conclude by drawing together all findings from the thesis to demonstrate how a comprehensive understanding of cognitive processes within the brain necessitates ‘what,’ ‘where,’ and crucially, ‘when’ information. I discuss how this thesis provides evidence of parallel processing pathways, and the likely presence of top-down predictions arising from this structure. I discuss the crucial role of the orbitofrontal cortex in salient face processing, and advance a new theoretical model for salient face processing that unites ‘cuteness ignition’ with current theoretical top-down models of object processing.
... projections was also studied with retrogradely transported fluorescent dyes, Harries and Perrett (1991) Marshall, 1993;Rizzolatti & Berti, 1993). Of particular interest for my argument, the typical lesion in such patients is far away from the ventral areas thought to be involved in face and gaze perception. ...
Orienting our own attention in the same direction as another person is a common example of social attention. Gaze direction and its perception offer an effective way to signal or perceive someone's current interest. Past accounts of gaze perception emphasised just geometrical cues from the seen eye. But human eyes have a unique morphology, with a large white surround (sclera) to the dark iris that may have evolved to enhance gaze processing. A series of new experiments show that the contrast polarity of seen eyes has a powerful influence on gaze perception. Adult observers are highly inaccurate in judging gaze direction for images of human eyes with negative contrast polarity, regardless of whether the surrounding face is shown in positive or negative polarity. The detrimental effect of negative contrast polarity is much larger for gaze perception than for other directional judgements (e.g. seen head direction). Cueing effects from seen gaze on the direction of the observer's own attention is also reduced for negative polarity eye stimuli. These results suggest an "expert" system for gaze perception, invariably treating the darker region of a seen eye as the part that does the looking. Further experiments show that gaze cues can interact with cues to head angle in determining gaze perception, in a manner that depends on time pressure. New evidence is also brought for possible right-hemisphere specialisation in gaze perception, as observers are more influenced by the left visual field eye than the right eye in a seen image. Finally, studies of gaze perception in a right-parietal patient with neglect suggest that some aspects of gaze perception can be relatively preserved even when awareness of the left eye is impaired.
... Electrophysiological and neuropsychological evidence highlighted the relationship between gaze direction and attention, indicating the existence of a specific neural substrate devoted to process meaningful gaze direction (i.e., gaze directed toward an object rather than toward empty space), like the superior temporal sulcus (STS; Allison, Puce, & McCarthy, 2000;Hoffman & Haxby, 2000;Pelphrey, Singerman, Allison, & McCarthy, 2003;Perrett et al., 1985). The STS projects input-output connections from-and to the fronto-parietal attentional networks (Corbetta, Miezin, Shulman, & Petersen, 1993;Maurizio & Shulman, 2002;Harries & Perrett, 1991;Nobre et al., 1997;Rafal, 1996). Through these connections, information about gaze direction projects to spatial attention systems to orient attention in the corresponding direction, as it occurs in joint attention. ...
This paper reviews methods to investigate joint attention, and highlights the benefits of new methodological approaches that make use of most recent technological developments such as humanoid robots for studying social cognition. After reviewing classical approaches addressing joint attention mechanisms with the use of controlled screen-based stimuli, we describe recent accounts that propose the need for more natural and interactive experimental protocols. Although the recent approaches allow for more ecological validity, they often face the challenges of experimental control in more natural social interaction protocols. In this context, we propose that the use of humanoid robots in interactive protocols is a particularly promising avenue to target the mechanisms of joint attention. Using humanoid robots to interact with humans in naturalistic experimental setups has the advantage of both excellent experimental control and ecological validity. In clinical applications, it offers new techniques for diagnosis and therapy, especially for children with Autism Spectrum Disorder. The review concludes with indications for future research, in the domain of healthcare applications and human-robot interaction in general.
... Electrophysiological and neuropsychological evidence highlighted the relationship between gaze direction and attention, indicating the existence of a specific neural substrate devoted to process meaningful gaze direction (i.e., gaze directed toward an object rather than toward empty space), like the superior temporal sulcus (STS; Allison, Puce, & McCarthy, 2000;Hoffman & Haxby, 2000;Pelphrey, Singerman, Allison, & McCarthy, 2003;Perrett et al., 1985). The STS projects input-output connections from-and to the fronto-parietal attentional networks (Corbetta, Miezin, Shulman, & Petersen, 1993;Maurizio & Shulman, 2002;Harries & Perrett, 1991;Nobre et al., 1997;Rafal, 1996). Through these connections, information about gaze direction projects to spatial attention systems to orient attention in the corresponding direction, as it occurs in joint attention. ...
This article reviews methods to investigate joint attention and highlights the benefits of new methodological approaches that make use of the most recent technological developments, such as humanoid robots for studying social cognition. After reviewing classical approaches that address joint attention mechanisms with the use of controlled screen-based stimuli, we describe recent accounts that have proposed the need for more natural and interactive experimental protocols. Although the recent approaches allow for more ecological validity, they often face the challenges of experimental control in more natural social interaction protocols. In this context, we propose that the use of humanoid robots in interactive protocols is a particularly promising avenue for targeting the mechanisms of joint attention. Using humanoid robots to interact with humans in naturalistic experimental setups has the advantage of both excellent experimental control and ecological validity. In clinical applications, it offers new techniques for both diagnosis and therapy, especially for children with autism spectrum disorder. The review concludes with indications for future research, in the domains of healthcare applications and human–robot interaction in general.
... Faces provide a rich source of social information (e.g., identity, gender, age, mental perspectives and emotional states), the processing of which is supported by specialised brain regions [1][2][3][4][5] . The accurate perception of social information in faces enables us to effectively understand the perspectives of conspecifics. ...
The human brain has evolved specialised mechanisms to enable the rapid detection of threat cues, including emotional face expressions (e.g., fear and anger). However, contextual cues – such as gaze direction – influence the ability to recognise emotional expressions. For instance, anger paired with direct gaze, and fear paired with averted gaze are more accurately recognised compared to alternate conjunctions of these features. It is argued that this is because gaze direction conveys the relevance and locus of the threat to the observer. Here, we used continuous flash suppression (CFS) to assess whether the modulatory effect of gaze direction on emotional face processing occurs outside of conscious awareness. Previous research using CFS has demonstrated that fearful facial expressions are prioritised by the visual system and gain privileged access to awareness over other expressed emotions. We hypothesised that if the modulatory effects of gaze on emotional face processing occur also at this level, then the gaze-emotion conjunctions signalling self-relevant threat will reach awareness faster than those that do not. We report that fearful faces gain privileged access to awareness over angry faces, but that gaze direction does not modulate this effect. Thus, our findings suggest that previously reported effects of gaze direction on emotional face processing are likely to occur once the face is detected, where the self-relevance and locus of the threat can be consciously appraised.
... Single-cell recordings in the macaque superior temporal sulcus (STS) have identified cells which are preferentially tuned to respond to specific views of a head (Harries & Perrett, 1991;Perret, Mistlin, & Chitty, 1989;). ...
... This region has been associated with visual-spatial attention, in particular attentional shifts (Corbetta, 1998;Corbetta et al., 1995;Haxby et al., 1994). Further, temporal-parietal connections may play a role in transferring expressive, changeable facial features (e.g., facial expressions, gaze directions) from the temporal to the parietal regions for spatial attention (Harries and Perrett, 1991). This might partially explain the difference noted between the parietal ROI and the occipito-temporal ROI. ...
Social information processing is a critical mechanism underlying children’s socio-emotional development. Central to this process are patterns of activation associated with one of our most salient socioemotional cues, the face. In this study, we obtained fMRI activation and high-density ERP source data evoked by parallel face dot-probe tasks from 9-to-12-year-old children. We then integrated the two modalities of data to explore the neural spatial-temporal dynamics of children’s face processing. Our results showed that the tomography of the ERP sources broadly corresponded with the fMRI activation evoked by the same facial stimuli. Further, we combined complementary information from fMRI and ERP by defining fMRI activation as functional ROIs and applying them to the ERP source data. Indices of ERP source activity were extracted from these ROIs at three a priori ERP peak latencies critical for face processing. We found distinct temporal patterns among the three time points across ROIs. The observed spatial-temporal profiles converge with a dual-system neural network model for face processing: a core system (including the occipito-temporal and parietal ROIs) supports the early visual analysis of facial features, and an extended system (including the paracentral, limbic, and prefrontal ROIs) processes the socio-emotional meaning gleaned and relayed by the core system. Our results for the first time illustrate the spatial validity of high-density source localization of ERP dot-probe data in children. By directly combining the two modalities of data, our findings provide a novel approach to understanding the spatial-temporal dynamics of face processing. This approach can be applied in future research to investigate different research questions in various study populations.
... Справедливости ради стоит сказать, что выводы о скученности нейронов, селективным к лицам, были сделаны ранее учеными, использовавшими только классический метод регистрации отдельных нейронов и гистологические методы. Еще в 1991 году Дэвид Пэрретт с коллегами обнаружил участки коры в височной доле макак, где доля нейронов, селективных к лицам, была намного выше, чем в соседних регионах [Harries, Perrett, 1991]. Они обнаружили несколько участков нервной ткани диаметром 3-5 мм в коре вокруг верхней височной борозды (superior temporal sulcus, STS), клетки в которых были более чувствительны к изображениям лиц, предвосхитив последующее открытие системы патчей в височной доле. ...
For intraspecific communication animals use signals of different modality: visual, auditory, chemosensory
etc. Crustaceans, insects, fish, amphibians, avians and mammals are capable to recognize conspecifics. Many vertebrates discriminate conspecifics from one another and modify behavior depending on social rank, status and kinship. In primates face recognition plays a critical role in social behavior which is provided by neurons of inferior temporal cortex. Temporal lobe in humans and macaques has similar functional organization. This cortical area contains several patches selective to faces and each of those has its own function. Information processing in the patches of inferior temporal cortex occurs hierarchically and in caudorostral direction face and body parts integrate into holistic representation of the whole agent. Inferior temporal cortex takes part in a network of brain structures coding various aspects of social interactions which also contains cingulate gyrus, parietal cortex, pulvinar, amygdala, claustrum and prefrontal cortex. In the nearest future combination of modern methods will lead to intriguining results in the field of neural networks processing social signals.
... Three different types of learned representations are included in the CogEM circuit of Figure 2(a): invariant object categories respond selectively to objects that are seen from multiple views, positions, and distances from an observer. They are learned by inferotemporal (IT) cortical interactions between anterior IT (ITa), posterior IT (ITp), and prestriate cortical areas like V4 (Figure 1; Desimone, 1998;Gochin et al., 1991;Harries and Perrett, 1991;Mishkin, 1982;Mishkin et al., 1983;Seger and Miller, 2010;Ungerleider and Mishkin, 1982). How such invariant object categories may be learned as the eyes scan a scene is modelled by the ARTSCAN Search neural model that is discussed in Sections 3.28 and 3.29 Chang et al., 2014;Fazl et al., 2009). ...
Background:
The prefrontal cortices play an essential role in cognitive-emotional and working memory processes through interactions with multiple brain regions.
Methods:
This article further develops a unified neural architecture that explains many recent and classical data about prefrontal function and makes testable predictions.
Results:
Prefrontal properties of desirability, availability, credit assignment, category learning, and feature-based attention are explained. These properties arise through interactions of orbitofrontal, ventrolateral prefrontal, and dorsolateral prefrontal cortices with the inferotemporal cortex, perirhinal cortex, parahippocampal cortices; ventral bank of the principal sulcus, ventral prearcuate gyrus, frontal eye fields, hippocampus, amygdala, basal ganglia, hypothalamus, and visual cortical areas V1, V2, V3A, V4, middle temporal cortex, medial superior temporal area, lateral intraparietal cortex, and posterior parietal cortex. Model explanations also include how the value of visual objects and events is computed, which objects and events cause desired consequences and which may be ignored as predictively irrelevant, and how to plan and act to realise these consequences, including how to selectively filter expected versus unexpected events, leading to movements towards, and conscious perception of, expected events. Modelled processes include reinforcement learning and incentive motivational learning; object and spatial working memory dynamics; and category learning, including the learning of object categories, value categories, object-value categories, and sequence categories, or list chunks.
Conclusion:
This article hereby proposes a unified neural theory of prefrontal cortex and its functions.
... The STS is the cortical site that has most consistently been implicated in the processing of BM (see Yovel & O'Toole, 2016, for a review). The STS is reciprocally connected with parietal cortex, which is known to play a key role in overt and covert orienting of attention (Harries & Perrett, 1991;Rafal, 1996). Although speculative, it remains plausible that unconscious attentional facilitation and inhibition by BM involves a neural circuit encompassing STS and parietal cortex that is sensitive to life-motion signals and guides attentional exploration in a temporally biphasic fashion. ...
... These three cortical areas, which constitute the MNS, the STS, area PF and area F5, are reciprocally connected. In the macaque monkey, area F5 in the premotor cortex is reciprocally connected to area PF (Luppino et al. 1999) creating a premotor-parietal MNS and STS is reciprocally connected to area PF of the inferior parietal cortex (Harries and Perrett 1991;Seltzer and Pandya 1994) providing a sensory input to the MNS (see Keysers and Perrett 2004 for a review). Furthermore, these reciprocal connections show regional specificity. ...
Is it possible to understand the intentions of other people by simply observing their actions? Many believe that this ability is made possible by the brain's mirror neuron system through its direct link between action and observation. However, precisely how intentions can be inferred through action observation has provoked much debate. Here we suggest that the function of the mirror system can be understood within a predictive coding framework that appeals to the statistical approach known as empirical Bayes. Within this scheme the most likely cause of an observed action can be inferred by minimizing the prediction error at all levels of the cortical hierarchy that are engaged during action observation. This account identifies a precise role for the mirror system in our ability to infer intentions from actions and provides the outline of the underlying computational mechanisms.
... M. Tipper, Handy, Giesbrecht, & Kingstone, 2008). The STS has dense connections to the intraparietal sulcus (IPS), which is important in covert attention shifts and spatial processing (Corbetta et al., 1998;Harries & Perrett, 1991;Materna, Dicke, & Thier, 2008;Rafal, 1996). The role of these connections has found support in studies that have correlated STS activation with activity in IPS under conditions where averted gaze (i.e., where gaze is directed away from the observer) is viewed (George, Driver, & Dolan, 2001;Pelphrey, Singerman, Allison, & McCarthy, 2003;Wicker, Michel, Henaff, & Decety, 1998). ...
Despite considerable interest in both action perception and social attention over the last 2 decades, there has been surprisingly little investigation concerning how the manual actions of other humans orient visual attention. The present review draws together studies that have measured the orienting of attention, following observation of another’s goal-directed action. Our review proposes that, in line with the literature on eye gaze, action is a particularly strong orienting cue for the visual system. However, we additionally suggest that action may orient visual attention using mechanisms, which gaze direction does not (i.e., neural direct mapping and corepresentation). Finally, we review the implications of these gaze-independent mechanisms for the study of attention to action. We suggest that our understanding of attention to action may benefit from being studied in the context of joint action paradigms, where the role of higher level action goals and social factors can be investigated.
... Its connectivity results range from AM, visual cortex, FG (MACM and RSFC analyses) and right pSTS (MACM) to the higher-level regions AI, SMG, and MTG (MACM). This concurs with the described model of FG connectivity to an extra-striate core system for face perception and a distributed, extended system for gaze perception and spatial attention (Mishkin M et al. 1983;Harries M and D Perrett 1991;Colby . Appraisal and binding of environmental input carrying social information is modulated by the NAC, a major node for motivation and reward (Schultz W 2004;Knutson B and JC Cooper 2005). ...
Social skills probably emerge from the interaction between different neural processing levels. However, social neuroscience is fragmented into highly specialized, rarely cross-referenced topics. The present study attempts a systematic reconciliation by deriving a social brain definition from neural activity meta-analyses on social cognitive capacities. The social brain was characterized by meta-analytic connectivity modeling evaluating coactivation in task-focused brain states and physiological fluctuations evaluating correlations in task-free brain states. Network clustering proposed a functional segregation into i) lower sensory, ii) limbic, iii) intermediate, and iv) high associative neural circuits that together mediate various social phenomena. Functional profiling suggested that no brain region or network is exclusively devoted to social processes. Finally, nodes of the putative mirror-neuron system were coherently cross-connected during tasks and more tightly coupled to embodied simulation systems rather than abstract emulation systems. These first steps may help reintegrate the specialized research agendas in the social and affective sciences.
... Stosunkowo niewiele wiadomo o anatomii czynnościowej układu wzrokowego u człowieka, ale przyjmuje się, że jest podobny do funkcjonującego u małp[53,99], że strumieniowi grzbietowemu odpowiada droga olbrzymiokomórka (M-pathway), zaś strumieniowi brzusznemu droga drobnokomórkowa (P-pathway). Pierwsza odpowiada za przetwarzanie informacji o lokalizacji i ruchu widzianych obiektów (pole V5), zaś druga o ich kształcie i kolorze (pole V4)[47]. Schemat dróg wzrokowych pokazano na poniższej rycinie (Ryc.5).stwierdzili, że światło czerwone jest bardziej efektywne, ale nie wszyscy badacze się z tym zgadzali[92]. ...
STRESZCZENIE
Podjęcie badań nad współzależnością aktywności bioelektrycznej mózgu i czynności bioelektrycznej serca znajduje uzasadnienie w aktualnym stanie wiedzy o mechanizmach regulacji w centralnym i autonomicznym układzie nerwowym oraz wpisuje się w wyraźny trend rozwoju współczesnej elektrofizjologii - dążenia do integracji badań aktywności bioelektrycznej różnych struktur anatomicznych i czynnościowych. Ten trend spowodował powstanie około 30 lat temu nowej dziedziny wiedzy, nazywanej w piśmiennictwie coraz częściej „neurokardiologią”. W Stanach Zjednoczonych Ameryki Północnej utworzone zostało centrum badawcze Institute of HeartMath, w którym prowadzone są badania nad fizjologicznymi mechanizmami interakcji mózgu i serca.
W pracy podjąłem badania dotyczące jednego z elementów współzależności mechanizmów regulacji w centralnym i autonomicznym układzie nerwowym, a mianowicie dotyczące poszukiwania zależności między zmianami aktywności bioelektrycznej mózgu i serca spowodowanymi stymulacją bodźcami zewnętrznymi – fotostymulacją.
Celem pracy było badanie zmienności rytmów korowych i zmienności rytmu serca w czasie fotostymulacji. W hipotezie badawczej pracy przyjęto, że fotostymulacja ma wpływ na zmiany aktywności bioelektrycznej mózgu i serca poprzez ośrodki układu autonomicznego odpowiedzialne za modulacje akcji serca.
Badania wykonano w Wojskowym Instytucie Medycyny Lotniczej w Środowiskowej Pracowni Neurofizjologii Ośrodkowego Układu Nerwowego. Badaną grupę stanowiło 20 mężczyzn w wieku 25-46 lat (średnia 36 lat). Badania polegały na jednoczesnej rejestracji sygnału EEG i EKG w czasie spoczynku i stymulacji światłem czerwonym i białym. Badanych podzielono na dwie grupy : z przewagą niskich lub wysokich częstotliwości widmie HRV.
Sygnał EEG był rejestrowany z 24 elektrod, rozmieszczonych na powierzchni czaszki w systemie 10-20. Zapis EKG rejestrowano ze standardowego odprowadzenia V5. W czasie rejestracji wykonywana była stymulacja lampą błyskową, umieszczoną w odległości 60 cm od oczu badanego, światłem czerwonym, a następnie białym. Energia bodźca wynosiła 0,5 J, a czas jego trwania 40 µs. Bodziec podawany był w seriach po 64 powtórzenia, co 2 sekundy (częstotliwość 0,5 Hz). Powyższy model stymulacji wybrano z uwagi na to, że jednym
z elementów oceny czynności bioelektrycznej serca była analiza widmowa wymagająca co najmniej 2 minutowego ciągłego zapisu EKG.
W wyniku przeprowadzonych badań stwierdzono, że fotostymulacja powodowała wzrost mocy widma HRV w zakresie niskich częstotliwości (LF) w obu badanych grupach. Stwierdzono istotne różnice w zmienności parametrów sygnału EEG i EKG w czasie stymulacji światłem czerwonym i białym. Ponadto, występowały istotne trendy w zmienności tych parametrów badanych sygnałów w czasie stymulacji światłem białym i czerwonym, ale nie stwierdzono istotnych korelacji (badanych testem Pearsona i Spearmana).
Wyniki wskazują na istotne, jednoczasowe zmiany sygnałów EEG i EKG, ale nie dają podstaw do rozważania ich wzajemnego wpływu. Mogą jednak stanowić przesłankę do kontynuowania badań nad współzależnością zmian czynności bioelektrycznej mózgu i serca oraz stanowić wskazówki dla kierunków dalszych badań. Sugerują, że ich istotnym elementem powinno być zapewnienie większej jednorodności badanej grupy osób oraz uwzględnienie morfologii zapisów EEG.
ABSTRACT
Undertaking research on the interdependence of bioelectrical activity of brain and heart is justified by the status of recent knowledge of the mechanisms, which regulate activity in central and autonomic nervous system. This research also follows the development trend of modern electrophysiology that strives to integrate studies of bioelectric activity of various anatomical structures. About 30 years ago, this trend formed the basis for creation of a new discipline of medicine, described in the literature as “neurocardiology".
Institute of HeartMath – a research center devoted to conducting studies on physiological relationships between brain and heart was established in the United States of America (in 1991 year).
In my work I carried out research of one of the aspects of interdependence between regulation mechanisms in central and autonomic nervous system. The research concentrated on the relationship between changes in bioelectrical activity of brain and heart caused by external stimulants – photic stimulation.
The aim of this work was to assess the variability of brain rhythms and heart rate during photic stimulation. It was hypothesized that photic stimulation has influence on changes of bioelectrical activity of brain and heart, through autonomic centers which control the heart rhythm.
Studies were performed in the Military Institute of Aviation Medicine. The study group consisted of 20 healthy subjects aged 22-57 (mean 36 years). The studies consisted of simultaneous registration of EEG and ECG signals during rest periods and photic stimulation with red and white light. The study population was divided into two groups: one characterized by an advantage of low frequency components and the other by advantage of high frequency components in HRV spectrum.
EEG signal was registered from 24 electrodes attached to the skin of skull according to International System 10-20. ECG signal was registered from the standard V5 lead. During the registration of EEG and ECG signals photic stimulation (white and red light) was performed with a flicker located 60 centimeters away from subject’s eyes. Series of 64 stimuli was applied with a frequency of 0,5 Hz and intensity of 0,5 J.
The above mentioned model of the study was chosen because at least
2-minute segments of ECG signal were required for HRV analysis.
The study revealed that the power of low frequency components of HRV spectrum was increased in both groups during photic stimulation. Statistically significant changes in variability of EEG and ECG signal parameters during photic stimulation with white and red light was also observed. Additionally significant trends in changes of these signals during photic stimulation were demonstrated. Nevertheless, no statistically significant correlations were ascertained (using Pearson and Spearman tests).
The results of the study indicate that there are significant changes of EEG and ECG signals, but their influence on each other can’t be yet determined. However, the results may be a prerequisite to further research on the interdependence of changes in bioelectrical activity of brain and heart, providing advices and directions for further studies. The outcome of the study also suggests that ensuring greater homogeneity of the tests groups, as well as taking morphology of EEG recordings into account are important elements that should not be overlooked in this kind of research.
... Motor representations M control the read-out of actions. In particular, the S representations are thalamocortical or cortico-cortical representations of external events, including the object recognition categories that are learned by inferotemporal and prefrontal cortical interactions (Desimone, 1991(Desimone, , 1998Gochin, Miller, Gross, & Gerstein, 1991;Harries & Perrett, 1991;Mishkin, Ungerleider, & Macko, 1983;Ungerleider & Mishkin, 1982), and that are modeled by ART. Sensory representations temporarily store internal representations of sensory events, such as conditioned stimuli (CS) and unconditioned stimuli (US), in short-term memory via recurrent on-center off-surround networks that tend to conserve their total activity while they contrast-normalize, contrast-enhance, and store their input patterns in short-term memory ( Fig. 4a and b). ...
How do the hippocampus and amygdala interact with thalamocortical systems to regulate cognitive and cognitive-emotional learning? Why do lesions of thalamus, amygdala, hippocampus, and cortex have differential effects depending on the phase of learning when they occur? In particular, why is the hippocampus typically needed for trace conditioning, but not delay conditioning, and what do the exceptions reveal? Why do amygdala lesions made before or immediately after training decelerate conditioning while those made later do not? Why do thalamic or sensory cortical lesions degrade trace conditioning more than delay conditioning? Why do hippocampal lesions during trace conditioning experiments degrade recent but not temporally remote learning? Why do orbitofrontal cortical lesions degrade temporally remote but not recent or post-lesion learning? How is temporally graded amnesia caused by ablation of prefrontal cortex after memory consolidation? How are attention and consciousness linked during conditioning? How do neurotrophins, notably brain-derived neurotrophic factor (BDNF), influence memory formation and consolidation? Is there a common output path for learned performance? A neural model proposes a unified answer to these questions that overcome problems of alternative memory models.
... A particularly well-studied and readily measured process reflecting such categorical discrimination is face-specific processing. Neural reflections of this process have been most directly observed as enhancements of specific neural responses to face images relative to images of any other object category that are observed in functional modules of the ventral extrastriate and ventral temporal cortices in human and nonhuman primates (Allison et al., 1994;Harries & Perrett, 1991;Perrett, Hietanen, Oram, & Benson, 1992). In normal human observers, for example, face-specific responses ...
Perceptual information represented in the brain, whether a viewer is aware of it or not, holds the potential to influence subsequent behavior. Here we tracked a well-established event-related-potential (ERP) measure of visual-object-category processing, the face-specific ventrolateral-occipital N170 response, across conditions of perceptual awareness. To manipulate perceptual awareness, we employed the motion-induced-blindness (MIB) paradigm, in which covertly attended, static, visual-target stimuli that are superimposed on a globally moving array of distractors perceptually disappear and reappear. Subjects responded with a button press when the target images (faces and houses) actually physically occurred (and thus perceptually appeared) and when they perceptually reappeared after an MIB episode. A comparison of the face-specific N170 ERP activity (face-vs-house responses) revealed robust face-selective ERP activity for physically appearing images and no such activity for perceptual reappearances following MIB episodes, suggesting that face-specific processing had continued uninterrupted during MIB. In addition, electrophysiological activity preceding an actual appearance of a target image, collapsed across face and house image types, was compared to that preceding the perceptual reappearance of a continuously present image (following MIB). This comparison revealed a parietally distributed positive-polarity response that preceded only reappearances following MIB. Such a result suggests a possible role of parietally mediated attentional capture by the present-but-suppressed target in the reestablishment of perceptual awareness at the end of an MIB episode. The present results provide insight into the level of visual processing that can occur in the absence of awareness, as well as into the mechanisms underlying MIB and its influence on perceptual awareness.
... Reciprocal connections exist between cell populations in the superior bank of the superior temporal sulcus and the intraparietal sulcus that could mediate the transfer of information about gaze direction and head orientation to parietal neural systems for spatial attention 69 . In the monkey, parietal cortex plays a central role in spatial perception and attention 70,71 . ...
Face perception plays a central role in social communication and is, arguably, one of the most sophisticated visual perceptual skills in humans. The organization of neural systems for face perception has stimulated intense debate. This article presents an updated model of distributed human neural systems for face perception. It opens up with a discussion of the Core System for visual analysis of faces with an emphasis on the distinction between perception of invariant features for identity recognition and changeable features for recognition of facial gestures such as expression and eye gaze. The study analyses the roles of systems for the representation of emotion, for person knowledge, and for action understanding in face recognition and perception of expression and gaze. It presents systems that are of particular relevance for social communication and that are illustrative of how distributed systems are engaged by face perception. It concludes with a discussion of modularity and distributed processing in neural representation.
... Further structures guiding spatial attention and eye movements are the supplementary eye field (SEF) in area F7, PPC, the pulvinar, the amygdala, and the caudate nucleus [49], all of which we found to be connected with the core face-processing system. These connections may aid in relaying information about the direction of attention of others extracted from a visual analysis of eyes and faces into the attentional system [50], and stronger connectivity of face patches than of nearby object patches with areas such as the SEF may underlie the behavioral advantages in directing saccades [5] and drawing spatial attention towards faces [4]. Thus, the core face-processing system interfaces with attention and executive control systems through multiple functional routes. ...
Author Summary
Primates have evolved to transmit social information through their faces. Where and how the brain processes facial information received by the eyes we now understand quite well. Yet we do not know how this information is made available to other brain areas so that a face can evoke an emotion, activate the memory of a person, or draw attention. Here, to identify brain regions interacting with face areas, we performed whole-brain imaging in macaque monkeys, whose face-processing system we know best. We find that the core face-processing areas are connected to several other brain areas supporting socially, emotionally, and cognitively relevant functions. Together, they form an extended face-processing network, similar to what has been proposed for humans. This extended face-processing network intersects with a second large-scale network, the so-called “default mode network”, in a pattern stunningly similar to that in the human brain. This intersection identifies selectively those brain regions that implement the most high-level forms of social cognition, such as understanding others’ thoughts and feelings. Thus, the results of this novel approach to understanding the functional organization of the social brain point to a deep evolutionary heritage of human abilities for social cognition.
... Another possible source of illusory contour interference is surface properties of the image representation. The complete model proposes that BCS boundaries regulate the filling-in of surface properties, such as brightness, color, depth, and form, within a feature contour system, or FCS (Arrington, 1994; Cohen & Grossberg,1984;Grossberg& Todorovi6,1988;Paradiso & Nakayama, 1991).The BCS is proposedto occur in the interblob cortical stream and the FCS in the blob stream from LGN to extrastriate area V4 (DeYoe & van Essen, 1988).Both the BCS and the FCS are proposedto interact reciprocally with object recognition and spatial orientation and action systems (Grossberg, 1994) that exist in temporal cortex and parietal cortex (Desimone, 1991Desimone, , 1992 Desimone & Ungerleider, 1989; Fischer & Breitmeyer, 1987; Gochin, 1990; Gochin et al., 1991; Goodale & Milner, 1992; Harries & Perrett, 1991; Mountcastle et al., 1981; Ungerleider & Mishkin, 1982). These reciprocal interactions can draw attention to prescribed surface regions and boundary segmenta- tions. ...
This article introduces an experimental paradigm to selectively probe the multipie levels of visual processing that influence the formation of object contours, perceptual boundaries, and illusory contours. The experiments test the assumption that, to integrate contour information across space and contrast sign, a spatially short-range filtering process that is sensitive to contrast polarity inputs to a spatially long-range grouping process that pools signals from opposite contrast polarities. The stimuli consisted of thin subthreshold lines, flashed upon gaps between collinear inducers which potentially enable the formation of illusory contours. The subthreshold lines were composed of one or more segments with opposite contrast polarities. The polarity nearest to the inducers was varied to differentially excite the short-range filtering process. The experimental results are consistent with neurophysiological evidence for cortical mechanisms of contour processing.and with the Boundary Contour System model, which identifies the short-range filtering process with cortical simple cells, and the long-range grouping process with cortical bipole cells.
... Another possible source of illusory contour interference is surface properties of the image representation. The complete model proposes that BCS boundaries regulate the filling-in of surface properties, such as brightness, color, depth, and form, within a feature contour system, or FCS (Arrington, 1994;Cohen & Grossberg,1984;Grossberg& Todorovi6,1988;Paradiso & Nakayama, 1991).The BCS is proposedto occur in the interblob cortical stream and the FCS in the blob stream from LGN to extrastriate area V4 (DeYoe & van Essen, 1988).Both the BCS and the FCS are proposedto interact reciprocally with object recognition and spatial orientation and action systems (Grossberg, 1994) that exist in temporal cortex and parietal cortex (Desimone, 1991(Desimone, , 1992Desimone & Ungerleider, 1989;Fischer & Breitmeyer, 1987;Gochin, 1990;Gochin et al., 1991;Goodale & Milner, 1992;Harries & Perrett, 1991;Mountcastle et al., 1981;Ungerleider & Mishkin, 1982). These reciprocal interactions can draw attention to prescribed surface regions and boundary segmentations. ...
... The MNS is a network composed of the ventral premotor cortex/posterior IFG, the inferior parietal lobule, and the pSTS (Iacoboni & Dapretto, 2006). The pSTS is reciprocally connected to the inferior parietal lobule (Harries & Perrett, 1991;Seltzer & Pandya, 1994) which is in turn connected to the ventral premotor cortex/ posterior IFG (Luppino, Murata, Govoni, & Matelli, 1999): These areas are hierarchically organized and reciprocally connected (Kilner, Friston, & Frith, 2007). Furthermore, it has been shown that the densest projections from the AMG to the prefrontal cortex terminate in the medial and lateral prefrontal cortex in monkeys, which includes the IFG in humans (Amaral & Price, 1984). ...
To date, the unifying pathogenesis, or etiology, of autism spectrum disorders (ASDs) and Williams syndrome (WS) remains unknown, partly because of the broad variation of phenotypes and the heterogeneity of syndrome expression. In particular, in order to comprehend the etiological mechanisms of their characteristic behaviors, great importance should be placed on realizing how the neural networks of individuals with autistic disorders and WS are formed and work. As such, in this paper, cortical network abnormalities, based on data from a variety of research fields, are presented: psychopathological, histopathological, and clinicopathological studies, as well as structural (i.e., morphological) and functional magnetic resonance imaging studies, including functional connectivity analysis. Based on the structure of the network, we propose an etiology for ASD and WS. Finally, we explain a variety of symptoms of these two disorders, including social and nonsocial dysfunction, based on our proposed neural network.
... Along the same lines, it is likely that two different neural networks underpin visuomotor facilitation in TD children and children with ASC. The central reliance of TD children on the preceding action observation suggests that the superior temporal sulcus (STS), an area providing the visual input to the MNS (Harries & Perrett, 2007;Seltzer & Pandya, 1994), plays a central role. STS anatomical and functional abnormalities do have paramount implications on the ASC symptomatology, with particular reference to the impairment of socially relevant information processing (Adolphs, 2003). ...
... Most importantly, this effect was proposed to occur because the human brain may be specialized to shift attention in response to where other people are attending/looking. The brain mechanisms for this "gaze cueing" effect were hypothesized to involve parietal cortex, which is involved in spatial orienting, and the STS, with which parietal cortex is reciprocally connected (e.g., Harries & Perrett 1991). ...
The present review examines the neural-behavioral correlates of human social attention, with special regard to the neural mechanisms involved in processing gaze information and the functional impact of gaze direction on the spatial orienting of attention. Our review suggests that there is strong evidence that specific brain systems are preferentially biased toward processing gaze information, yet this specificity is not mirrored by the behavioral data as measured in highly controlled model attention tasks such as the Posner cueing paradigm. In less controlled tasks, however, such as when observers are left free to select what they want to attend, they focus on people and their eyes, consistent with one's intuition and with the neural evidence that eyes are special. We discuss a range of implications of these data, including that much is to be gained by examining brain and behavioral processes to social stimuli as they occur in complex real-world settings.
... In fact, many of these cells have been found to be simultaneously sensitive to head and body orientation, though they are preferentially sensitive to eye gaze (Perrett et al., 1985). Furthermore, reciprocal projections from the STS to the parietal cortex, implicated in the processing of spatial awareness (Harries & Perrett, 1991), suggest that gaze direction perception is obligatorily involved in reflexive orienting in the direction of another's gaze. Likewise, in humans similar STS and parietal activations have been documented during eye gaze detection . ...
Eyes hold special prominence in human exchange and have across time and culture. They serve both as a salient channel through which people send nonverbal messages as well as the primary mechanism by which people perceive nonverbal messages sent by others. An analysis of famous portraits dating back 5 centuries (Tyler, 1998) underscores the perceptual salience of eyes by showing that one eye was almost always painted on or very near the horizontal center of the portrait, presumably reflecting the inner character of the subject. Such an assumption matches popular folk wisdom that “the eyes are the window to our souls”—wisdom that has infiltrated people’s most personal and even most global of interactions. Although remaining silent on matters of the soul, contemporary science nevertheless strongly supports the claim that the eyes are a richly informative social cue, critical to people’s social exchange. For humans, the “language of the eyes” appears innately prepared. An ability to process gaze information is believed to play a pivotal role in the development of theory of mind—hat is, the ability to understand that others have mental and emotional experiences different than your own (Baron-Cohen, 2002), which is evidenced also by the fact that psychopathological disorders marked by deficits in theory of mind (e.g., autism) are likewise linked to a failure to attend to the eyes (Emery, 2000). Whether this “language” is universal remains open to question, although we often assume it is. Despite such assumptions, there are important individual, contextual, and cultural influences that can affect how people interpret messages conveyed by eyes. In this chapter, we explore eye behaviors, how and why people engage in them, what meanings people derive from them, and the factors that influence such perceptions. The first part of the chapter focuses on why people are drawn to the eyes. The second part focuses on two relatively less-studied eye behaviors: tear production and pupil dilation/constriction. The third part of the chapter focuses on the far more researched behavior of gaze, both as a channel for information gathering and as a critical mechanism for social signaling, including discussion of the role of gaze in theory of mind and emotion perception. A central assumption of all this work is that the eyes capture a disproportionate amount of attention compared to other aspects of nonverbal behavior, particularly considering their relatively small size. Before delving into eye behavior, therefore, we first review evidence that humans are exquisitely tuned to the eye region of the face.
... Such a dispersed pattern of activation might be expected to produce a random stippling of activation throughout the fusiform gyrus rather than the focal activation that we found. Alternatively, face-specific regions could occur in patches of cortex (perhaps composed of clusters of face-specific columns), an arrangement sug-gested by face-sensitive patches of cortex in monkey temporal lobe (Harries & Perrett, 1991). The right hemisphere activations in Figure 2e suggest elongated patches of face-specific cortex located in the midfusiform sulcus and lateral fusiform gyrus. ...
The perception of faces is sometimes regarded as a specialized task involving discrete brain regions. In an attempt to identi$ face-specific cortex, we used functional magnetic resonance imaging (fMRI) to measure activation evoked by faces presented in a continuously changing montage of common objects or in a similar montage of nonobjects. Bilateral regions of the posterior fusiform gyrus were activated by faces viewed among nonobjects, but when viewed among objects, faces activated only a focal right fusiform region. To determine whether this focal activation would occur for another category of familiar stimuli, subjects viewed flowers presented among nonobjects and objects. While flowers among nonobjects evoked bilateral fusiform activation, flowers among objects evoked no activation. These results demonstrate that both faces and flowers activate large and partially overlapping regions of inferior extrastriate cortex. A smaller region, located primarily in the right lateral fusiform gyrus, is activated specifically by faces.
... When coarse matches are allowed, a top-down expectation, say from prefrontal to inferotemporal cortex, can learn a prototype that is capable of focusing attention on general and abstract information. When only fine matches are allowed, learned prototypes are more specific and concrete and can focus attention even on individual exemplars, such as particular views of particular faces (Desimone and Ungerleider, 1989;Gochin et al., 1991;Harries and Perrett, 1991). ...
The concept of attention has been used in many senses, often without clarifying how or why attention works as it does. Attention, like consciousness, is often described in a disembodied way. The present article summarizes neural models and supportive data about how attention is linked to processes of learning, expec- tation, competition, and consciousness. A key theme is that attention modulates cortical self-organization and stability. The perceptual and cognitive neocortex is organized into six main cell layers, with characteris- tic sublamina. Attention is part of a unified design of bottom-up, horizontal, and top-down interactions among identified cells in laminar cortical circuits. Neural models clarify how attention may be allocated during processes of visual perception, learning, and search; auditory streaming and speech perception; movement target selection during sensory-motor control; mental imagery and fantasy; and hallu- cinations during mental disorders, among other processes.
The human visual system has evolved specialized neural mechanisms to rapidly detect faces. Its broad tuning for facial features is thought to underlie the illusory perception of faces in inanimate objects, a phenomenon called face pareidolia. Recent studies on face pareidolia suggest that the mechanisms underlying face processing, at least at the early stages of visual encoding, may treat objects that resemble faces as real faces; prioritizing their detection. In our study, we used breaking continuous flash suppression (b-CFS) to examine whether the human visual system prioritizes the detection of objects that induce face pareidolia over stimuli matched for object content. Similar to previous b-CFS results using real face stimuli, we found that participants detected the objects with pareidolia faces faster than object-matched control stimuli. Given that face pareidolia has been more frequently reported amongst individuals prone to hallucinations, we also explored whether this rapid prioritization is intact in individuals with schizophrenia, and found evidence suggesting that it was. Our findings suggest that face pareidolia engages a broadly tuned mechanism that facilitates rapid face detection. This may involve the proposed fast subcortical pathway that operates outside of visual awareness.
Introduction
Faces provide a rich source of social information, crucial for the successful navigation of daily social interactions. People with schizophrenia suffer a wide range of social-cognitive deficits, including abnormalities in face perception. However, to date, studies of face perception in schizophrenia have primarily employed tasks that require patients to make judgements about the faces. It is, thus, unclear whether the reported deficits reflect an impairment in encoding visual face information, or biased social-cognitive evaluative processes.
Methods
We assess the integrity of early unconscious face processing in 21 out-patients diagnosed with Schizophrenia or Schizoaffective Disorder (15M/6F) and 21 healthy controls (14M/7F). In order to control for any direct influence of higher order cognitive processes, we use a behavioural paradigm known as breaking continuous flash suppression (b-CFS), where participants simply respond to the presence and location of a face. In healthy adults, this method has previously been used to show that upright faces gain rapid and privileged access to conscious awareness over inverted faces and other inanimate objects.
Results
Here, we report similar effects in patients, suggesting that the early unconscious stages of face processing are intact in schizophrenia.
Conclusion
Our data indicate that face processing deficits reported in the literature must manifest at a conscious stage of processing, where the influence of mentalizing or attribution biases might play a role.
This paper reviews the literature on social neuroscience studies using macaques in the hope of encouraging as many researchers as possible to participate in this field of research and thereby accelerate the system-level understanding of social cognition and behavior. We describe how different parts of the primate brain are engaged in different aspects of social information processing, with particular emphasis on the use of experimental paradigms involving more than one monkey in laboratory settings. The description begins with how individual neurons are used for evaluating socially relevant information, such as the identity, face, and focus of attention of others in various social contexts. A description of the neural bases of social reward processing and social action monitoring follows. Finally, we provide several perspectives on novel experimental strategies to help clarify the nature of interacting brains under more socially and ecologically plausible conditions.
The “speed of thought” may be measured in a number of ways by different disciplines (such as by cognitive psychologists and neuropsychologists). However, only the neurophysiologist is able to go to the heart of the matter; the speed of the response of neurons. Such investigations provide crucial information for all researchers working on how the brain works, as it allows them to base their ideas in a biologically plausible framework. However, almost all approaches to interpreting a neuron’s response examine long time samples of the response, usually around 300–500 msec. Is this a biologically plausible length of time? We know that it is possible to recognize and respond to a visual stimulus within 400–600 msec. If one considers that at least half of this time is involved in the generation and implementation of motor commands, it means that the total amount of time available for processing in the whole visual system is considerably less than the period over which a cell’s response is conventionally measured. This book focuses on the relatively neglected issue of the importance of rapid processing, and how we should take this into account as we explore how information is processed in the visual system.
In the primary stages of the visual system, such as VI, objects are coded in terms of retinotopic coordinates, and lesions of VI cause defects in retinal space which move with eye movements, maintaining a constant retinal location. Several stages later in the visual system, at the inferior temporal cortex, the receptive fields are relatively independent of retinal location, and neurons can be activated by a specific stimulus, such as a face, over a wide range of retinal locations. Deficits that result from lesions of the inferior temporal cortex are based on the coordinate system properties of the object, independent of retinal location. Thus, at some point in the visual system, the pattern of excitation that reaches the eye must be transposed from a retinotopic coordinate system to a coordinate system centered on the object itself.1,2
Learning in the brain can be divided into implicit and explicit modes, where the former corresponds to skill learning or priming (or other types) and the latter to semantic or to episodic coding in which awareness of the memory is possible to the subject. The former type of learning is thought to take place in non-cortical regions (cerebellum, thalamus, etc.) and posterior associative cortex, the latter in associative cortex and more specifically in hippocampus (if only temporarily).
We review the properties of cells in the temporal cortex of the macaque monkey, which are sensitive to visual cues arising from the face and body and their movements. We speculate that the responses of populations of cells in the cortex of the anterior superior temporal sulcus (STSa) support an understanding of the behaviour of others. Actions of an agent including whole body movements (e.g. walking) and articulations (of the limbs and torso) made during the redirecting of attention and reaching are coded by STSa cells in a way which: (1) allows generalization over different views and orientations of the agent with respect to the observer, (2) utilises information about the agent's current and (3) imagined position while occluded from sight and (4) is sensitive to sequences of the agent's movements. The selectivity of cells is described from the perspective of hierarchical processing, which presumes that early processing establishes sensitivity to simple body cues and later coding combines these cues to specify progressively more subtle and abstract aspects of behaviour. The action coding of STSa cells is discussed in terms of dorsal and ventral cortical systems, the binding problem and the functional architecture, which allows hierarchical information processing.
This chapter reviews some of the work on the perception of gaze direction and shifting of attention, which is triggered by eye gaze. The evidence suggests that the excellent accuracy we display in perceiving gaze is underpinned by at least two mechanisms-one analyzing luminance contrast, the other performing a spatial computation on the eye's features-and must take into account the orientation of the gazer's head. Both of the mechanisms for perceiving gaze also seem to be involved in the generation of shifts of attention in the direction in which another's eyes are pointing and do so via dedicated neural circuitry. © 2011 by Reginald B. Adams, Jr., Nalini Ambady, Ken Nakayama, Shinsuke Shimojo. All rights reserved.
Introduction Neural responses to face stimuli may seem like an unwieldy subject for investigating population activity: neurons with face-selective responses are many synapses removed from sensory input, the coding for faces appears to be very sparse, and the stimuli are complex making “proper” control stimuli difficult to come by. So why bother? To the extent that population coding underlies certain cognitive abilities, then those activities that are biological imperatives for the animal should be given “neural priority.” In the rat, foraging and spatial localization relative to “home” points is one critical natural behavior. In primates, social cognition is essential. With the face at the heart of social communication and identification of social status, it should not come as a surprise that neurons appear to “care” about face stimuli in a way not seen for many non-face objects. But the nature of perceiving and learning about facial signals, in terms of population dynamics, is very under-explored territory. Surprisingly, in regions most often associated with face-selective responses, the conclusion of some researchers has been that population activity may add little to nothing to the perception of faces. The current state of knowledge regarding neural bases of face perception will be discussed. The role, if any, of population dynamics, will then be explored. Specifically, the population interactions of face-processing systems across space (e.g. circuits), and time (e.g. oscillations) will be discussed.
Human neuroimaging and event-related potential (ERP) studies suggest that ventral and lateral temporo-occipital cortex is sensitive to static faces and face parts. Recent fMRI data also show activation by facial movements. In this study we recorded from 22 posterior scalp locations in 20 normal right-handed males to assess ERPs evoked by viewing: (1) moving eyes and mouths in the context of a face; (2) moving and static eyes with and without facial context. N170 and P350 peak amplitude and latency data were analysed. N170 is an ERP previously shown to be preferentially responsive to face and eye stimuli, and P350 immediately follows N170. Major results were: (1) N170 was significantly larger over the bilateral temporal scalp to viewing opening mouths relative to closing mouths, and to eye aversion relative to eyes gazing at the observer; (2) at a focal region over the right inferior temporal scalp, N170 was significantly earlier to mouth opening relative to closing, and to eye aversion relative to eyes gazing at the observer; (3) the focal ERP effect of eye aversion occurred independent of facial context; (4) these differences cannot be attributable to movement per se, as they did not occur in a control condition in which checks moved in comparable areas of the visual field; (5) isolated static eyes produced N170s that were not significantly different from N170s to static full faces over the right inferior temporal scalp, unlike in the left hemisphere where face N170s were significantly larger than eye N170s; (6) unlike N170, P350 exhibited nonspecific changes as a function of stimulus movement. These results suggest that: (1) bilateral temporal cortex forms part of a system sensitive to biological motion, of which facial movements form an important subset; (2) there may be a specialised system for facial gesture analysis that provides input for neuronal circuitry dealing with social attention and the actions of others.
Human beings have remarkable social attention skills. From the initial processing of cues, such as eye gaze, head direction, and body orientation, we perceive where other people are attending, allowing us to draw inferences about the intentions, desires, and dispositions of others. But before we can infer why someone is attending to something in the world we must first accurately represent where they are attending. Here we investigate the "where" of social attention perception, and employ adaptation paradigms to ascertain how head and body orientation are visually represented in the human brain. Across two experiments we show that the representation of two cues to social attention (head and body orientation) exists at the category-specific level. This suggests that aftereffects do not arise from "social attention cells" discovered in macaques or from abstract representations of "leftness" or "rightness."
Four experiments investigate the hypothesis that cues to the direction of another's social attention produce a reflexive orienting of an observer's visual attention. Participants were asked to make a simple detection response to a target letter which could appear at one of four locations on a visual display. Before the presentation of the target, one of these possible locations was cued by the orientation of a digitized head stimulus, which appeared at fixation in the centre of the display. Uninformative and to-be-ignored cueing stimuli produced faster target detection latencies at cued relative to uncued locations, but only when the cues appeared 100 msec before the onset of the target (Experiments 1 and 2). The effect was uninfluenced by the introduction of a to-be-attended and relatively informative cue (Experiment 3), but was disrupted by the inversion of the head cues (Experiment 4). It is argued that these findings are consistent with the operation of a reflexive, stimulus-driven or exogenous orienting mechanism which can be engaged by social attention signals.
Classifying a face as male or female was shown to be reliably affected by the direction in which the face was looking-a variable apparently unrelated to reported features of the face that show sexual dimorphism. Decisions were slower when gaze was averted downwards. Furthermore, masculinity ratings were lower for men's faces looking down than for the same faces looking ahead. One high-level (configurational) face feature that varies with the sex of the face and with direction of gaze was identified. The vertical upper-lid-to-brow distance is smaller in men than in women and becomes less salient when eyes are averted down. This display feature may have evolved to signal gender quickly and reliably, especially in alert male faces.
Most vertebrates, humans included, have a primitive visual system extremely sensitive to the motion of biological entities. Most previous studies have examined the global aspects of biological motion perception, but local motion processing has received much less attention. Here we provide direct psychophysical and electrophysiological evidence that human observers are intrinsically tuned to the characteristics of local biological motion cues independent of global configuration. Using a modified central cueing paradigm, we show that observers involuntarily orient their attention towards the walking direction of feet motion sequences, which triggers an early directing attention negativity (EDAN) in the occipito-parietal region 100-160ms after the stimulus onset. Notably, such effects are sensitive to the orientation of the local cues and are independent of whether the observers are aware of the biological nature of the motion. Our findings unambiguously demonstrate the automatic processing of local biological motion without explicit recognition. More importantly, with the discovery that local biological motion signals modulate attention, we highlight the functional importance of such processing in the brain.
The cognition that constructs mental features such as intention, disposition, and character is an aspect of theory of mind. This aspect of representation of minds, which inherently has valence, is viewed from cognitive, evolutionary, and neural perspectives. It is proposed that this cognition is modular, and that it normally operates in association with a valence-free cognition able to represent mental states such as belief. Examples of neural activity capable of supporting the social representations macaque monkeys are believed to possess (understanding of affective displays, purposeful movement, and elemental social interactions) are presented.
Patient AMA suffered a head trauma that left her with several visual complaints, including a reading disability. AMA appears to suffer from simultanagnosia, as established with tasks such as naming briefly presented multiple stimuli or overlapping figures, describing the theme of complex scenes, and counting arrays of stimuli. Specifically, AMA has difficulty perceiving immediately successive stimuli and, in particular, multiple stimuli that appear at novel or unexpected locations. Her ability to encode spatial relations rapidly (of either the categorical and coordinate type) is markedly reduced. However, when a familiar target appears among multiple stimuli at expected (previously encoded) locations, AMA' s performance can be within normal limits. These results suggest that this patient' s simultanagnosia cannot be reduced to an inability to process multiple stimuli per se. Rather it is better characterised as (1) an inability to index new locations of multiple stimuli, and (2) a reduced efficiency in pattern analysis. The former deficit, in turn, may lead to difficulty in focusing on objects efficiently and using objects as landmarks or reference points. Damage to one or both of the above mechanisms could produce simultanagnosia and reading difficulty.
In order to gather evidence on functional subdivisions of the temporal lobe neocortex of the primate, the activity of more than 2600 single neurons was recorded in 10 myelo- and cytoarchitecturally defined subdivisions of the cortex in the superior temporal sulcus (STS) and inferior temporal gyrus of the anterior part of the temporal lobe of 5 hemispheres of 3 macaque monkeys. First, convergence of different modalities into each area was investigated. Areas TS and TAa, in the upper part of this region, were found to receive visual as well as auditory inputs. Areas TPO, PGa, and IPa, in the depths of the STS, received visual, auditory, and somatosensory inputs. Areas TEa, TEm, TE3, TE2, and TE1, which extend from the ventral bank of the STS through the inferior temporal gyrus, were primarily unimodal visual areas. Second, of the cells with visual responses, it was found that some neurons in areas TS-IPa could be activated only by moving visual stimuli, whereas the great majority of neurons in areas TEa-TE1 could be activated by stationary visual stimuli. Third, it was found that there were few sharply discriminating visual neurons in areas TS and TAa; of the sharply discriminating visual neurons in other areas, however, neurons that responded primarily to faces were found predominantly in areas TPO, TEa, and TEm (in which they represented 20% of the neurons with visual responses); neurons that were tuned to relatively simple visual stimuli such as sine-wave gratings, color, or simple shapes were relatively common in areas TEa, TEm, and TE3; and neurons that responded only to complex visual stimuli were common in areas IPa, TEa, TEm, and TE3. These findings show inter alia that areas TPO, PGa, and IPa are multimodal, that the inferior temporal gyrus areas are primarily unimodal, that there are areas in the cortex in the anterior and dorsal part of the STS that are specialized for the analysis of moving visual stimuli, that neurons responsive primarily to faces are found predominantly in areas TPO, TEa, and TEm, and that architectural subdivisions of the temporal lobe cortex are related to neuronal response properties.
In the primate visual system, the identification of objects and the processing of spatial information are accomplished by different cortical pathways. The computational properties of this "two-systems" design were explored by constructing simplifying connectionist models. The models were designed to simultaneously classify and locate shapes that could appear in multiple positions in a matrix, and the ease of forming representations of the two kinds of information was measured. Some networks were designed so that all hidden nodes projected to all output nodes, whereas others had the hidden nodes split into two groups, with some projecting to the output nodes that registered shape identity and the remainder projecting to the output nodes that registered location. The simulations revealed that splitting processing into separate streams for identifying and locating a shape led to better performance only under some circumstances. Provided that enough computational resources were available in both streams, split networks were able to develop more efficient internal representations, as revealed by detailed analyses of the patterns of weights between connections.
A variety of cell types exist in the temporal cortex providing high-level visual descriptions of bodies and their movements. We have investigated the sensitivity of such cells to different viewing conditions to determine the frame(s) of reference utilized in processing. The responses of the majority of cells in the upper bank of the superior temporal sulcus (areas TPO and PGa) found to be sensitive to static and dynamic information about the body were selective for one perspective view (e.g. right profile, reaching right or walking left). These cells can be considered to provide viewer-centred descriptions because they depend on the observer's vantage point. Viewer-centred descriptions could be used in guiding behaviour. They could also be used as an intermediate step for establishing view-independent responses of other cell types which responded to many or all perspective views selectively of the same object (e.g. head) or movement. These cells have the properties of object-centred descriptions, where the object viewed provides the frame of reference for describing the disposition of object parts and movements (e.g. head on top of shoulders, reaching across the body, walking forward 'following the nose'). For some cells in the lower bank of the superior temporal sulcus (area TEa) the responses to body movements were related to the object or goal of the movements (e.g. reaching for or walking towards a specific place). This goal-centred sensitivity to interaction allowed the cells to be selectively activated in situations where human subjects would attribute causal and intentional relationships.
The direction of eye gaze and orientation of the face towards or away from another are important social signals for man and for macaque monkey. We have studied the effects of these signals in a region of the macaque temporal cortex where cells have been found to be responsive to the sight of faces. Of cells selectively responsive to the sight of the face or head but not to other objects (182 cells) 63% were sensitive to the orientation of the head. Different views of the head (full face, profile, back or top of the head, face rotated by 45 degrees up to the ceiling or down to the floor) maximally activated different classes of cell. All classes of cell, however, remained active as the preferred view was rotated isomorphically or was changed in size or distance. Isomorphic rotation by 90-180 degrees increased cell response latencies by 10-60 ms. Sensitivity to gaze direction was found for 64% of the cells tested that were tuned to head orientation. Eighteen cells most responsive to the full face preferred eye contact, while 18 cells tuned to the profile face preferred averted gaze. Sensitivity to gaze was thus compatible with, but could be independent of, sensitivity to head orientation. Results suggest that the recognition of one type of object may proceed via the independent high level analysis of several restricted views of the object (viewer-centred descriptions).
V5 and V4 are areas of macaque monkey prestriate visual cortex that are specialized for involvement in different aspects of visual perception, namely motion for V5 (refs 1-4) and colour vision, with other possible functions, for V4 (refs 2, 5-9). Thus, it is unlikely that they should be fed the same information for further processing, yet both receive a strong input from patches of the upper layers of V2 (refs 10, 11), the area immediately adjoining the primary visual cortex, V1. V2, however, seems to comprise functionally distinct subregions, which can be revealed by staining the tissue for the mitochondrial enzyme cytochrome oxidase. Here we report that V4 and V5 are connected with separate cytochrome oxidase-defined subregions of V2, suggesting that cortical pathways dealing with motion and colour perception are segregated in their passage through V2, and reinforcing evidence for functional specialization in the visual cortex.
Patterns of anatomical connections in the visual cortex form the structural basis for segregating features of the visual image into separate cortical areas and for communication between these areas at all levels to produce a coherent percept. Such multi-stage integration may be a common strategy throughout the cortex for producing complex behaviour.
In order to gather evidence on functional subdivisions of the temporal lobe neocortex of the primate, the activity of more than 2600 single neurons was recorded in 10 myelo- and cytoarchitecturally defined subdivisions of the cortex in the superior temporal sulcus (STS) and inferior temporal gyrus of the anterior part of the temporal lobe of 5 hemispheres of 3 macaque monkeys. First, convergence of different modalities into each area was investigated. Areas TS and TAa, in the upper part of this region, were found to receive visual as well as auditory inputs. Areas TPO, PGa, and IPa, in the depths of the STS, received visual, auditory, and somatosensory inputs. Areas TEa, TEm, TE3, TE2, and TE1, which extend from the ventral bank of the STS through the inferior temporal gyrus, were primarily unimodal visual areas. Second, of the cells with visual responses, it was found that some neurons in areas TS-IPa could be activated only by moving visual stimuli, whereas the great majority of neurons in areas TEa-TE1 could be activated by stationary visual stimuli. Third, it was found that there were few sharply discriminating visual neurons in areas TS and TAa; of the sharply discriminating visual neurons in other areas, however, neurons that responded primarily to faces were found predominantly in areas TPO, TEa, and TEm (in which they represented 20% of the neurons with visual responses); neurons that were tuned to relatively simple visual stimuli such as sine-wave gratings, color, or simple shapes were relatively common in areas TEa, TEm, and TE3; and neurons that responded only to complex visual stimuli were common in areas IPa, TEa, TEm, and TE3. These findings show inter alia that areas TPO, PGa, and IPa are multimodal, that the inferior temporal gyrus areas are primarily unimodal, that there are areas in the cortex in the anterior and dorsal part of the STS that are specialized for the analysis of moving visual stimuli, that neurons responsive primarily to faces are found predominantly in areas TPO, TEa, and TEm, and that architectural subdivisions of the temporal lobe cortex are related to neuronal response properties.
Movement provides biologically important information about the nature (and intent) of animate objects. We have studied cells in the superior temporal sulcus of the macaque monkey which seem to process such visual information. We found that the majority of cells in this brain region were selective for type of movement and for stimulus form, most cells responding only to particular movements of the body or some part of it. A variety of cell types emerged, including cells sensitive to: translation of bodies in view, movements into view (appearance) or out of view (disappearance) and the articulation and rotation of the body/head. Directional selectivity for cells sensitive to translation tended to lie along one of 3 orthogonal Cartesian axes centred on the monkey (towards/away, left/right and up/down). One type of rotation sensitive cell was tuned to rotation about one or more of these axes, a second type was sensitive to different head rotations which brought the face to confront the monkey or turned the face away. Reconstructions of cell positions indicated that cells of the same type were clumped anatomically both across the surface of the cortex and perpendicular to the surface.
Monkeys deprived of their visual cortex (area 17) have been thought to be unable to discriminate much more than ``total luminous energy''. In particular, they have been considered incapable of localizing visual events in space. It has now been shown that they can be trained to detect and accurately reach out for objects of certain kinds presented visually.
Versuche an „split-brain“ Affen legten die Annahme nahe, daß die Wahrnehmung des Raumes und die Wahrnehmung der Identität von Gegenständen auf anatomisch getrennten Hirnmechanismen beruhen. In der vorliegenden Arbeit werden die Sehmechanismen des Gehirns untersucht, wobei von der Überlegung ausgegangen wird, daß hier zwei parallele Prozesse involviert sind: ein dezentrierter („ambient“), der die Wahrnehmung des den Körper umgebenden Raumes bestimmt, und ein zentrierter („focal“), durch welchen Details kleiner Raumflächen aufgefaßt werden.
Bei Wirbeltieren wird eine detaillierte Topographie des körper-zentrierten Verhaltensraumes vom Auge zum Mittelhirn projiziert. Diese visuelle Topographie ist so mit dem bi-symmetrischen motorischen System integriert, daß sich eine Korrespondenz zwischen gesehenen Punkten und Bewegungszielen ergibt.
Das phylogenetisch jüngere visuelle System des Vorderhirns befaßt sich fast ausschließlich mit dem zentralen Verhaltensraum; die corticale motorische Kontrolle befaßt sich entsprechend mit sehr spezifischen Handlungen im gleichen zentralen Gebiet.
Anatomie und Hirnchirurgie liefern bei Primaten Hinweise auf einen visuellen Mechanismus im Mittelhirn, der für die dezentrierte Raumwahrnehmung eine Rolle spielt. Im Gegensatz dazu greift das auf Fovea, Parafovea und den visuellen Arealen des Cortex beruhende zentrierte Sehen Areale des umgebenden Feldes für eine eingehendere Inspektion heraus. Koordinierte Augenbewegungen sind direkter Ausdruck dieser Aufmerksamkeitszuwendung.
Die Wechselwirkung zweier Mechanismen der visuellen Analyse kennzeichnet das Sehen bei allen aktiven Tieren. Die Komplexität des zentrierten Sehens zeigt sich auf allen Stufen des visuellen Systems von Primaten und in den Teilen des motorischen Systems, welche das Sehen ausrichten und die auf bestimmte visuelle Objekte gerichteten Handlungen steuern.
Staining for the mitochondrial enzyme cytochrome oxidase reveals an array of dense regions (blobs) in the primate primary visual cortex. They are most obvious in the upper layers, 2 and 3, but can also be seen in layers 4B, 5, and 6, in register with the blobs in layers 2 and 3. We compared cells inside and outside blobs in macaque and squirrel monkeys, looking at their physiological responses and anatomical connections. Cells within blobs did not show orientation selectivity, whereas cells between blobs were highly orientation selective. Receptive fields of blob cells had circular symmetry and were of three main types, Broad-Band Center-Surround, Red-Green Double-Opponent, and Yellow-Blue Double-Opponent. Double-Opponent cells responded poorly or not at all to white light in any form, or to diffuse light at any wavelength. In contrast to blob cells, none of the cells recorded in layer 4C beta were Double-Opponent: like the majority of cells in the parvocellular geniculate layers, they were either Broad-Band or Color-Opponent Center-Surround, e.g., red-on-center green-off-surround. To our surprise cells in layer 4C alpha were orientation selective. In tangential penetrations throughout layers 2 and 3, optium orientation, when plotted against electrode position, formed long, regular, usually linear sequences, which were interrupted but not perturbed by the blobs. Staining area 18 for cytochrome oxidase reveals a series of alternating wide and narrow dense stripes, separated by paler interstripes. After small injections of horseradish peroxidase into area 18, we saw a precise set of connections from the blobs in area 17 to thin stripes in area 18, and from the interblob regions in area 17 to interstripes in area 18. Specific reciprocal connections also ran from thin stripes to blobs and from interstripes to interblobs. We have not yet determined the area 17 connections to thick stripes in area 18. In addition, within area 18 there are stripe-to-stripe and interstripe-to-interstripe intrinsic connections. These results suggest that a system involved in the processing of color information, especially color-spatial interactions, runs parallel to and separate from the orientation-specific system. Color, encoded in three coordinates by the major blob cell types, red-green, yellow-blue, and black-white, can be transformed into the three coordinates, red, green, and blue, of the Retinex algorithm of Land.
Of 497 single neurones recorded in the cortex in the fundus of the superior temporal sulcus (STS) of three alert rhesus monkeys, a population of at least 48 cells which were selectively responsive to faces had the following response properties: (1) The cells' responses to faces (real or projected, human or rhesus monkey) were two to ten times as large as those to gratings, simple geometrical stimuli or complex 3-D objects. (2) Neuronal responses to faces were excitatory, sustained and were time-locked to the stimulus presentation with a latency of between 80 and 160 ms. (3) The cells were unresponsive to auditory or tactile stimuli and to the sight of arousing or aversive stimuli. (4) The magnitude of the responses of 28 cells tested was relatively constant despite transformations, such as rotation, so that the face was inverted or horizontal, and alterations of colour, size or distance. (5) Rotation to profile substantially reduced the responses of 21 cells (31 tested). (6) Masking out or presenting parts of the face (i.e. eyes, mouth or hair) in isolation revealed that different cells responded to different features or subsets of features. (7) For several cells, responses to the normal organisation of cut-out or line-drawn facial features were significantly larger than to jumbled controls. These findings indicate that explanations in terms of arousal, emotional or motor reactions, simple visual feature sensitivity or receptive fields are insufficient to account for the selective responses to faces and face features observed in this population of STS neurones. It appears that these neurones are part of a system specialised to code for faces or features present in faces, and it is suggested that damage to this system is related to prosopagnosia, or difficulty in face recognition, in man and to the tameness and social disturbances which follow temporal lobe damage and are part of the Klüver-Bucy syndrome in the monkey.
The disadvantage of the present methods for the staining of myelin sheaths—Weigert, Spielmeyer, Loyez, Fränkel and others—is that they require days or even weeks for the preparation of the material.
The following method can be performed within one hour and can be applied to sections fixed in formaldehyde and frozen or embedded in either celloidin or paraffin. Celloidin sections may be stained without removing the embedding material. In paraffin sections, the paraffin should be removed before staining. Frozen sections should be brought into 70 per cent alcohol for from five to ten minutes and then put back into water. Sections should be from 20 to 30 microns thick.
The agents used are: (1) 5 per cent water solution of potassium dichromate; (2) 4 per cent water solution of iron alum; (3) 1 per cent water solution of hematoxylin prepared from 10 per cent absolute alcoholic solution (at least 6
The organization of primate primary visual cortex has been shown to be highly compartmented by the new neuroanatomical techniques of 2-deoxyglucose, cytochrome oxidase staining, and neurotransmitter immunocytochemistry. In Old World monkeys the ocular dominance columns (ODC) are continued into layers above layer IV, but are subdivided into a cytochrome oxidase-heavy system of circular patches or dots which are aligned along the centers of the ODC, and a cytochrome oxidase-light region which spans the ODC borders. New World monkeys also possess a system of cytochrome oxidase dots, despite their lack of ODC. Anatomical labelling and electrophysiological recording indicate that each cytochrome oxidase subdivision probably processes a different type of visual information and has a separate connectivity with prestriate cortex.
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Conducted 2 experiments that examined the behavioral significance of tactile and motion sensitive cells in the superior temporal sulcus (STS) of the macaque brain. In the awake, behaving monkey, the critical dimension for polymodal coding was whether or not the sensations were expected. Tactile stimulation out of sight could not be predicted and elicited neuronal responses. By contrast, when the monkey could see and, therefore, predict impending contact, or when the monkey touched a familiar surface in a predictable location, cell responses were reduced or abolished. In an analogous way some cells were unresponsive to the sight of the monkey's own limbs moving, but responded to the sight of other moving stimuli. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Posterior parietal cortex has traditionally been considered to be a sensory association area in which higher-order processing and intermodal integration of incoming sensory information occurs. In this paper, evidence from clinical reports and from lesion and behavioral-electrophysiological experiments using monkeys is reviewed and discussed in relation to the overall functional organization of posterior parietal association cortex, and particularly with respect to a proposed posterior parietal mechanism concerned with the initiation and control of certain classes of eye and limb movements. Preliminary data from studies of the effects of posterior parietal lesions on oculomotor control in monkeys are reported.
The behavioral effects of lesions of posterior parietal cortex in monkeys have been found to be similar to those which follow analogous damage of the minor hemisphere in humans, while behavioral-electrophysiological experiments have disclosed classes of neurons in this area which have functional properties closely related to the behavioral acts that are disrupted by lesions of the area. On the basis of current data from these areas of study, it is proposed that the sensory association model of posterior parietal function is inadequate to account for the complexities of the present evidence. Instead, it now appears that many diverse neural mechanisms are located in part in parietal cortex, that some of these mechanisms are involved in sensory processing and perceptual functions, but that others participate in motor control, and that still others are involved in attentional, motivational, or emotional processes. It is further proposed that the elementary units of these various neural mechanisms are distributed within posterior parietal cortex according to the columnar hypothesis of Mountcastle.
The experiments described in this study were intended to increase our knowledge about social cognition in primates. Longtailed macaques (Macaca fascicularis) had to discriminate facial drawings of different emotional expressions. A new experimental approach was used. During the experimental sessions social interactions within the group were permitted, but the learning behaviour of individual monkeys was analysed. The procedure consisted of a simultaneous discrimination between four visual patterns under continuous reinforcement. It has implications not only for simple tasks of stimulus discrimination but also for complex problems of internal representations and visual communication.
The monkeys learned quickly to discriminate faces of different emotional expressions. This discrimination ability was completely invariant with variations of colour, brightness, size, and rotation. Rotated and inverted faces were recognized perfectly. A preference test for particular features resulted in a graded estimation of particular facial components. Most important for face recognition was the outline, followed by the eye region and the mouth. An asymmetry in recognition of the left and right halves of the face was found. Further tests involving jumbled faces indicated that not only the presence of distinct facial cues but the specific relation of facial features is essential in recognizing faces. The experiment generally confirms that causal mechanisms of social cognition in non-human primates can be studied experimentally. The behavioural results are highly consistent with findings from neurophysiology and research with human subjects.
We have examined callosal-axon neurons giving rise to homotopic and heterotopic callosal projections to caudal inferior parietal lobule (area PG) in Macaca mulatta, identifying these neurons by means of retrograde axonal transport of horseradish peroxidase. The labeled neurons in the homotopic region occur predominantly in layers IIIB and V. A moderate number are seen also in layer VI, a smaller number in layer IV, and rare cells occur in layer II. These neurons occupy a region very similar in outline to the injection area, and though variable in density in the horizontal plane are continuously distributed in this plane.
The heterotopic neurons are seen in the contralateral cingulate gyrus, continuing caudally into medial parietal cortex, in the cortex of the superior temporal and occipitotemporal sulci, in the caudal superior temporal gyrus, and in the caudal inferior parietal lobule, behind the homotopic area. These same regions on the ipsilateral side contain labeled neurons of origin of ipsilateral association projections to area PG. For other ipsilateral association regions (e.g., frontal lobe), no corresponding contralateral heterotopic labeling was found. A review of the literature on heterotopic callosal connections allows tentative generalization of this conclusion: The callosal heterotopic connections of a particular cortical area are made with regions which on the ipsilateral side have association connections with that area, though usually not with all of such regions.
The laminar and tangential distributions of association neurons projecting from areas 4 and 6 of the frontal lobe to area 5 of the superior parietal lobule were studied in macaque monkeys by using horseradish peroxidase histochemistry. In both areas 4 and 6 association neurons were medium-large pyramidal cells of layers II and III, and pyramidal and fusiform cells of layers V-VI. Tangentially, they were distributed unevenly over the cortical surface occupying only certain parts of areas 4 and 6, including the dorsomedial part of area 6, the proximal arm region of Woolsey's M1 map, parts of the postarcuate cortex, and the supplementary motor area. Within these projection zones, the number of projection cells waxed and waned in a periodic fashion.
Quantitative methods, including spectral analysis techniques, were used to characterize precisely spatial periodicities along the rostrocaudal dimension. The same quantitative analyses were used to determine the nature of the tangential distribution of corticocallosal cells of area 5 projecting to contralateral area 5. Both association and callosal spectra contained a strong component in the range of low spatial frequencies, corresponding to periods greater than 2 mm. Moreover, a consistent peak was observed in both spectra at spatial frequencies corresponding to periods ranging from 0.85 to 1.28 mm. This peak is in accord with the hypothesis of a modular organization of the cells of origin of these projection systems.
The striate cortex of the macaque monkey is subdivided into two independent and overlapping systems of columns termed “orientation columns” and “ocular dominance columns.” The present paper is concerned with the orientation columns, particularly their geometry and the relationship between successive columns. The arrangement of the columns is highly ordered; in the great majority of oblique or tangential microelectrode penetrations the preferred orientations of cells changed systematically with electrode position, in a clockwise or counterclockwise direction. Graphs of orientation vs. electrode track distance were virtually straight lines over distances of up to several millimeters; such orderly sequences were often terminated by sudden changes in the direction of orientation shifts, from clockwise to counterclockwise or back. The orientations at which these reversals occurred were quite unpredictable. Total rotations of 180–360° were frequently seen between reversals. In tangential or almost tangential penetrations orientation shifts occurred almost every time the electrode was moved forward, indicating that the columns were either not discrete or had a thickness of less than 25–50 μ, the smallest order of distance that our methods could resolve. In penetrations that were almost perpendicular to the surface, the graphs of orientation vs. track distance were relatively flatter, as expected if the surfaces of constant orientation are perpendicular to the cortical surface. Stepwise changes in orientation of about 10° could sometimes be seen in perpendicular penetrations, each orientation persisting through several clear advances of the electrode, suggesting a set of discrete columnar subdivisions. The possibility of some kind of continuous variation in orientation with horizontal distance along the cortex was not, however, completely ruled out. Occasionally a highly ordered sequence was broken by an abrupt large shift in orientation of up to 90°. Shifts in ocular dominance occurred roughly every 0.25–0.5 mm and were independent of orientation shifts. In multiple parallel penetrations spaced closer than about 250 μ the slopes of the orientation vs. track distance curves were almost the same; reconstruction of these penetrations indicated that the regions of constant orientation are parallel sheets. On crossing perpendicular to these sheets, a total orientation shift of 180° took place over a distance of 0.5–1.0 mm. Column thickness, size of shifts in orientation, and the rate of change of orientation with distance along the cortex seemed to be independent of eccentricity, at least between 2° and 15° from the fovea. A few penetrations made in area 17 of the cat and in area 18 of the monkey showed similar orderly sequences of receptive-field orientation shifts.
Single cell recordings in monkey striate cortex have shown differences in response properties from one cell layer to the next and have also shown that the IVth layer, which receives most of its input from the geniculate, is subdivided into a mosaic of regions, some connected to the left eye, others to the right. In the present study small lesions were made in single layers or pairs of layers in the lateral geniculate body, and the striate cortex was later examined with a Fink‐Heimer modification of the Nauta method. We hoped to correlate the laminar distribution of axon terminals in the cortex with functional differences between layers, and to demonstrate the IVth‐layer mosaic anatomically.
After lesions in either of the two most dorsal (parvocellular) layers, terminal degeneration was found mainly in layer IVc, with a second minor input to a narrow band in the upper part of IVa. A very few degenerating fibers ascended to layer I. In contrast, lesions in either of the two ventral (magnocellular) layers were followed by terminal degeneration confined, apparently, to IVb, or at times extending for a short distance into the upper part of IVc; no degeneration was seen in layer IVa or in layer I.
After a lesion confined to a single geniculate layer, a section through the corresponding region of striate cortex showed discrete areas or bands of degeneration in layer IV, usually 0.5–1.0 mm long, separated by interbands of about the same extent in which there was no terminal degeneration. When serial sections were reconstructed to obtain a face‐on view of the layer‐IV mosaic, it appeared as a series of regular, parallel, alternating degeneration‐rich and degeneration‐poor stripes. When a geniculate lesion involved both layer VI (the most dorsal, with input from the contralateral eye) and the part of layer V directly below (ipsilateral eye), the cortical degeneration, as expected, occupied a virtually continuous strip in layer IVc and the reconstructed face‐on view of this layer showed a large confluent region of degeneration.
In some of the reconstructions the cortical stripes seemed highly regular; in others there was a variable amount of cross connection between stripes. The stripes varied in width from 0.25 to 0.50 mm, and width did not seem to correlate with region of retinal representation.
It is concluded that the long narrow stripes of alternating left‐eye and right‐eye input to layer IV are an anatomical counterpart of the physiologically observed ocular‐dominance columns. Because of this segregation of inputs, cells of layer IV are almost invariably influenced by one eye only. A cell above or below layer IV will be dominated by the eye supplying the nearest IVth layer stripe, but will generally, though not always, receive a subsidiary input from the other eye, presumably by diagonal connections from the nearest stripes supplied by that eye.
Populations of visual neurones have been discovered in one area of the temporal association cortex that respond to different aspects of facial information. The responses of these cells have many of the properties hypothesized for ‘gnostic units’ and provide insight into the final stages of visual processing leading to recognition of an object as a face and more specifically the identity of the face.
Evidence is reviewed indicating that striate cortex in the monkey is the source of two multisynaptic corticocortical pathways. One courses ventrally, interconnecting the striate, prestriate, and inferior temporal areas, and enables the visual identification of objects. The other runs dorsally, interconnecting the striate, prestriate, and inferior parietal areas, and allows instead the visual location of objects. How the information carried in these two separate pathways is reintegrated has become an important question for future research.
The combined use of two anterograde axonal transport methods reveals that in the prefrontal association cortex of macaque
monkeys, associational projections from the parietal lobe of one hemisphere interdigitate with callosal projections from the
opposite frontal lobe, forming adjacent columns 300 to 750 micrometers wide. The finding of separate and alternating ipsilateral
and contralateral inputs in the frontal association cortex opens up new possibilities for the functional analysis of this
large but unexplored area of the primate brain.
An attempt is made at showing that the cerebral cortex has to be envisaged as a mosaic of columnar units of remarkably similar internal structure and surprisingly little variation of diameter (200-300 mu m). A systematic investigation is made of various types of interneurons and also of the local connections of the pyramidal cells by the combined application of four techniques: (i) the classical Golgi procedures, (ii) electron microscope studies of various types of synapses, (iii) light and electron microscope studies in chronically isolated cortical slabs of the local synapses that persist under such circumstances, and (iv) serial reconstruction-under the electron microscope-of clearly identified Golgi-stained interneurons (and pyramidal cells) which has revealed a hitherto unexpected degree of specificity in local connectivity. Most interneurons are not only highly specific with respect to the arborization pattern of their axons and to the size and shape within which they establish synapses with specific sites of certain other neurons, but also with respect to the character, preferential localization, and origin of the synapses that they receive. On the basis of this kind of information the local neuron network of the cerebral cortex can be defined as an intricate system of repetitive but mutually interpenetrating spatial modules of specific interneuron arborizations. As a consequence the synapses of each individual interneuron are distributed in such geometrically defined modules of cortical space. Some of the interneuron types and the corresponding spatial modules can be identified with considerable confidence as being of an excitatory, and others of an inhibitory, nature. By using recent information on the mode of termination of various afferent pathways of the cortex and on the cellular origin of the main efferent pathways, tentative models for the cortical neuron chains can be proposed.
Since the first reports of aggregations by ocular dominance of ceils in monkey striate cortex'-', :~, the geometry of these groupings has become increasingly clear. The columns have been reconstructed anatomically, first using the Wiitanen modification of the Nauta-Fink-Heime r method~, 9, then by autoradiography tMlowing eye in- jection of labeled material s, and finally by a reduced silver method staining tangentially running fibers in layer IV C v. All of these methods show that the aggregations as seen in a face-on, surface view are actually parallel stripes with varying number~, of cross- linkages, bifurcations and blind endings. Fig. 1A gives an example of such a reconstruction made from serial sections stained by the reduced silver method (adapted from ref. 7, Fig. 8a); it shows the entire exposed surface of a macaque monkey's right occipital lobe, representing a region of visual field that extends from the fovea out to about 9". i n Fig. l A alternate stripes have been inked in to show the two-fold nature of the subdivisions; the dark stripes can be imagined to represent the projections of the left eye onto layer 1V C and the light stripes the projections of the right eye, or the reverse: in this animal we made no re- cordings and hence do not know which set corresponded to the left eye and which to the right. The continuation of the stripes into the calcarine fissure is shown in Fig. t B and C; here again alternate stripes are inked in, and again the choice of which set to show as dark is arbitrary. These fragments extend the reconstruction out to about 25 '~, A narrow gap between the three pieces, about 1 mm wide, occurs at the folds where the cortex was sectioned at an angle that was too far from tangential to allow the fiber bands to be seen. Our object in the present study was to learn roughly how the cortical stripes would appear if transposed into the visual field. Certain predictions can be made from what is already known. A conspicuous feature of the anatomical stripes is the constancy of their width, about 400/zm, from the fovea out almost as far as the monocular crescent s. The representation of the visual fields on the cortex is far from uniform, however: it is detailed in the foveal region and becomes coarser with eccentricity. As transformed
A cyto- and myeloarchitectonic parcellation of the superior temporal sulcus and surrounding cortex in the rhesus monkey has been correlated with the pattern of afferent cortical connections from ipsilateral temporal, parietal and occipital lobes, studied by both silver impregnation and autoradiographic techniques. The results suggest a definite organization of this region. Subdivisions of the superior temporal gyrus are tied together in a precise sequence of connections beginning in primary auditory cortex. The inferotemporal area, which receives input from the lateral peristriate region, can also be divided into architectonic divisions, each of which is related to the others in a specific pattern of connections. Within the superior temporal sulcus several distinct areas exist. In the caudal reaches is found a region that receives input from both primary visual and visual association cortices. This zone is similar to the Clare-Bishop area of the cat. Other superior temporal sulcus zones receive input primarily from one limited area of association cortex. A strip in the upper bank receives input exclusively from the superior temporal gyrus. An area in the rostral lower bank has afferent connections mainly with the inferotemporal area, and a zone in the depth of the superior temporal sulcus receives fibers from a region within the lower bank of the intraparietal sulcus. Two additional zones, in the upper bank of the superior temporal sulcus, however, have multiple sources of cortical input: the peristriate belt, inferior parietal lobule and caudal superior temporal gyrus.
V2 is a visual area of the macaque monkey which is at the second level in a recently proposed hierarchy of cortical visual areas. Histochemical staining for cytochrome oxidase (CO) in V2 reveals a pattern of alternate thick and thin CO-rich stripes separated by CO-sparse interstripes. These subregions receive distinct inputs from neurones in CO-rich and CO-sparse zones arrayed within the superficial layers of V1 (refs 4, 5). Are output projections from V2 to higher visual areas also segregated? Using an anatomical double-label paradigm, we have now demonstrated that V2 cells projecting to two of its major target areas, MT and V4 (refs 6, 7), are arranged in stripe-like clusters which are largely segregated from one another and which are closely related to the pattern of CO stripes. Concomitant electrophysiological recordings from V2 indicate that groups of cells having similar receptive field properties are clustered within the subregions defined by these anatomical techniques.
The primate visual cortex is a quilt of different areas, each having characteristic anatomical and functional features. The interpretation of the organization of these areas and their function in perception has been a subject of intense debate. New impetus has been given to this debate through the serendipitous discovery that the metabolic enzyme, cytochrome oxidase, is distributed in precise patterns within some areas. This discovery led to the hypothesis that the enzyme is a marker of separate routes of processing through the cortical visual areas. If true, this would be a remarkable development in our understanding of the neural basis of visual perception. It thus seems a timely moment at which to analyse the genesis of this hypothesis and its experimental support.
Neurophysiological studies have shown that some neurons in the cortex in the superior temporal sulcus and in the inferior temporal cortex respond to faces. To determine if some face responsive neurons encode stimuli in an object-centered coordinate system rather than a viewer-centered coordinate system, a large number of neurons were tested for sensitivity to head movement in 3 macaque monkeys. Ten neurons responded only when a head undergoing rotatory movements was shown. All of these responded to a particular movement independently of the orientation of the moving head in relation to the viewer, maintaining specificity even when the moving head was inverted or shown from the back, thereby reversing viewer-centered movement vectors. This was taken as evidence that the movement was encoded in object-centered coordinates. In tests of whether there are neurons in this area which respond differently to the faces of different individuals relatively independently of viewing angle, it was found that a further 18 neurons responded more to one static face than another across different views. However, for 16 of these 18 cells there was still some modulation of the neuronal response with viewing angle. These 16 neurons thus did not respond perfectly in relation to the object shown independently of viewing angle, and may represent an intermediate stage between a viewer-centered and an object-centered representation. In the same area as these neurons, other cells were found which responded on the basis of viewer-centered coordinates. These neurophysiological findings provide evidence that some neurons in the inferior temporal visual cortex respond to faces (or heads) on the basis of object-centered coordinates, and that others have responses which are intermediate between object-centered and viewer-centered representations. The results are consistent with the hypothesis that object-centered representations are built in the inferior temporal visual cortex.
Experimental and clinical studies have generally shown that the neural mechanisms for face processing in man are (1) designed to deal with the configuration of upright faces and (2) located predominantly in the right cerebral hemisphere. Monkeys would seem to process faces in a different manner to humans since they appear to show no hemispheric asymmetry and to treat upright and inverted faces equivalently. We re-examine these claims. Our reaction time studies reveal that monkeys do behave like human subjects since they process facial configuration faster when stimuli are presented upright as compared with horizontal or inverted. Single unit studies in the monkey reveal patches of neurones responsive to faces in the upper bank and fundus of the left superior temporal sulcus (STS). Recording from the right hemisphere also reveals cells responsive to faces but in this hemisphere such cells appear less numerous. These cells process upright faces faster than inverted faces. Face processing in monkeys and man appears to utilize qualitatively similar mechanisms, but the extent and/or direction of cerebral asymmetry in these mechanisms may not be similar.
The retrogradely transported fluorescent tracers True Blue and Diamidino Yellow were compared. They were found similar in the following respects: spread at injection sites; uptake from fibres of passage; fading of fluorescence and absence of retrograde transneuronal transport. Their fluorescence properties were, however, dissimilar and this, rather than differences in their sensitivity or efficiency, appears to account for their differences in respect of the intensities of fluorescence in such labelled neurones.
Voltage-sensitive dyes allow neuronal activity to be studied by non-invasive optical techniques. They provide an attractive means of investigating striate cortex, where important response properties are organized in two dimensions. In the present study, patterns of ocular dominance and orientation selectivity were obtained repeatedly from the same patch of cortex using the dye merocyanine oxazolone, together with current image-processing techniques. The patterns observed agree with most established features of monkey striate cortex and suggest a new unit of cortical organization; one that is modular in structure and which appears to link the organization of orientation selectivity with that of ocular dominance.
1. The striate cortex was studied in lightly anaesthetized macaque and spider monkeys by recording extracellularly from single units and stimulating the retinas with spots or patterns of light. Most cells can be categorized as simple, complex, or hypercomplex, with response properties very similar to those previously described in the cat. On the average, however, receptive fields are smaller, and there is a greater sensitivity to changes in stimulus orientation. A small proportion of the cells are colour coded.
2. Evidence is presented for at least two independent systems of columns extending vertically from surface to white matter. Columns of the first type contain cells with common receptive‐field orientations. They are similar to the orientation columns described in the cat, but are probably smaller in cross‐sectional area. In the second system cells are aggregated into columns according to eye preference. The ocular dominance columns are larger than the orientation columns, and the two sets of boundaries seem to be independent.
3. There is a tendency for cells to be grouped according to symmetry of responses to movement; in some regions the cells respond equally well to the two opposite directions of movement of a line, but other regions contain a mixture of cells favouring one direction and cells favouring the other.
4. A horizontal organization corresponding to the cortical layering can also be discerned. The upper layers (II and the upper two‐thirds of III) contain complex and hypercomplex cells, but simple cells are virtually absent. The cells are mostly binocularly driven. Simple cells are found deep in layer III, and in IV A and IV B. In layer IV B they form a large proportion of the population, whereas complex cells are rare. In layers IV A and IV B one finds units lacking orientation specificity; it is not clear whether these are cell bodies or axons of geniculate cells. In layer IV most cells are driven by one eye only; this layer consists of a mosaic with cells of some regions responding to one eye only, those of other regions responding to the other eye. Layers V and VI contain mostly complex and hypercomplex cells, binocularly driven.
5. The cortex is seen as a system organized vertically and horizontally in entirely different ways. In the vertical system (in which cells lying along a vertical line in the cortex have common features) stimulus dimensions such as retinal position, line orientation, ocular dominance, and perhaps directionality of movement, are mapped in sets of superimposed but independent mosaics. The horizontal system segregates cells in layers by hierarchical orders, the lowest orders (simple cells monocularly driven) located in and near layer IV, the higher orders in the upper and lower layers.
In primate primary visual cortex, staining for cytochrome oxidase reveals a regular array of blob-like structures, most prominent in layers II and III but also present in layers V and VI. In an attempt to learn more about the input to these blobs, we injected the lateral geniculate bodies of macaques and squirrel monkeys with [3H]proline or horseradish peroxidase and looked in the cortex for transported label. As expected, label was present in layers IVa, IVc alpha, IVc beta, and VI. In addition, both methods revealed an array of puffs deep in layer III. Seen in tangential sections, the puffs precisely matched the cytochrome blobs. These results indicate a projection from the lateral geniculate body to the blob regions deep in layer II/III, either indirect via layer IV or more likely direct. In area 18 stained for cytochrome oxidase, we also observed complex banding patterns; these were remarkably similar to the pattern found after [3H]proline or horseradish peroxidase injection and were also similar to the pattern produced with 2-deoxyglucose labeling after stimulation with vertical or horizontal stripes; the proline and peroxidase labels probably represent a projection from the pulvinar to area 18.
The functional organization of the second cortical visual area was examined with three different anatomical markers: 2-[14C]deoxy-D-glucose,
cytochrome oxidase, and various myelin stains. All three markers revealed strips running throughout the area, parallel to
the cortical surface. The boundaries of these strips provide an anatomical criterion for defining the borders of this extrastriate
region. Further, the demonstration of these strips allows a functional and anatomical analysis of modules in the area, just
as the recent demonstration of spots in the primary visual cortex has allowed an analysis of modules there. The strips differ
structurally and functionally from interstrip regions and these differences are similar to those seen between the spots and
the interspot regions in the primary visual cortex. In the macaque the strips and spots differ with regard to binocular organization.
We have investigated the distribution of cells responsive to faces within the macaque temporal cortex and their sensitivity to different face attributes. We found a functional organization of cells responsive to the sight of different views of the head. Cells of a similar type were grouped together both vertically down through the cortex, and horizontally in patches extending 0.5-2.0 mm across the surface of the cortex. A substantial proportion of cells responsive to faces were found to be sensitive to biologically important characteristics such as identity or expression. Cells were found to be highly selective for particular individuals that were familiar to the monkey with selectivity persisting across a great variety of viewing conditions such as changing face expression, orientation, colour, distance and size. Data suggested that sensitivity to identity arises at the level of specific views of the individual (e.g. full face). Information about different views may then be pooled to allow recognition independent of view. Visual transformations that make it difficult for humans to perceive faces (e.g., contrast reversal, isoluminant colour, coarsely quantized images, rotation or inversion) reduced the magnitude or increased the latency of cells' responses to faces. In this way, cell responses were related to perception and not simply to visual qualities of the image.
The origin, course, and termination of parieto-temporal connections in the rhesus monkey were studied by autoradiographic techniques. The caudal third of the inferior parietal lobule (including the adjacent lower bank of the intraparietal sulcus) is the chief source of these projections. It projects to three separate architectonic areas in the superior temporal sulcus and to three different areas on the ventral surface of the temporal lobe: the parahippocampal gyrus, presubiculum, and perirhinal cortex. The mid-inferior parietal lobule and medial surface of the parietal lobe, by contrast, project only to the caudal upper bank of the superior temporal sulcus. The rostral inferior parietal lobule and the superior parietal lobule, as well as the postcentral gyrus and rostral parietal operculum, do not project to the temporal lobe. Fibers travel from the posterior parietal region to temporal cortex by way of several different routes. One fiber bundle courses in the superior temporal gyrus and terminates in the superior temporal sulcus. Another proceeds ventrally, between the depth of the superior temporal sulcus and the geniculocalcarine tract, to the parahippocampal area. A separate bundle, coursing part of the way in the company of the cingulum bundle, conveys posterior parietal fibers to the presubiculum.
Viewer-centered and object centered encoding of heads by cells in the superior temporal sulcus of the rhesus monkey
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