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How Inferior Temporal Cortex Became a Visual Area
Abstract
The origins of contemporary work on the temporal cortex and object recognition are traced from their roots in phrenology through the search for a cortical visual area to the discovery of the Klüver-Bucy syndrome and its fractionation, finally ending with early single-neuron recording studies.
... Neurons in early visual areas in monkeys are tuned to simple features of the stimuli, such as the orientation of bars in area V1 or direction of motion in area V5. In the monkey inferotemporal cortex (IT), neurons respond to complex stimuli, including faces and hands, but also abstract patterns or common, everyday objects [1][2][3] . There are strong projections from IT to higher association areas in the temporal lobe, including the parahippocampal gyrus, perirhinal cortex, entorhinal cortex, hippocampus and amygdala 4,5 . ...
... The neuron did not respond to food items based on these five repetitions. articles studies in humans 18 , and from single-neuron electrophysiology [1][2][3] and lesions in monkeys 9,10,25 suggests a fundamental role for the medial temporal lobe in visual object recognition. Category-specific knowledge deficits occur in which neurological patients show impairments in identifying living things, objects, food items or faces 11,12,24 . ...
... Single inferotemporal cortex (IT) neurons in monkeys respond to complex visual stimuli, including faces, objects and abstract patterns [1][2][3] . Neurons in human temporal neocortex respond to faces and words 32,33 . ...
... Neurons in early visual areas in monkeys are tuned to simple features of the stimuli, such as the orientation of bars in area V1 or direction of motion in area V5. In the monkey inferotemporal cortex (IT), neurons respond to complex stimuli, including faces and hands, but also abstract patterns or common, everyday objects [1][2][3] . There are strong projections from IT to higher association areas in the temporal lobe, including the parahippocampal gyrus, perirhinal cortex, entorhinal cortex, hippocampus and amygdala 4,5 . ...
... The neuron did not respond to food items based on these five repetitions. articles studies in humans 18 , and from single-neuron electrophysiology [1][2][3] and lesions in monkeys 9,10,25 suggests a fundamental role for the medial temporal lobe in visual object recognition. Category-specific knowledge deficits occur in which neurological patients show impairments in identifying living things, objects, food items or faces 11,12,24 . ...
... Single inferotemporal cortex (IT) neurons in monkeys respond to complex visual stimuli, including faces, objects and abstract patterns [1][2][3] . Neurons in human temporal neocortex respond to faces and words 32,33 . ...
The hippocampus, amygdala and entorhinal cortex receive convergent input from temporal neocortical regions specialized for processing complex visual stimuli and are important in the representation and recognition of visual images. Recording from 427 single neurons in the human hippocampus, entorhinal cortex and amygdala, we found a remarkable degree of category-specific firing of individual neurons on a trial-by-trial basis. Of the recorded neurons, 14% responded selectively to visual stimuli from different categories, including faces, natural scenes and houses, famous people and animals. Based on the firing rate of individual neurons, stimulus category could be predicted with a mean probability of error of 0.24. In the hippocampus, the proportion of neurons responding to spatial layouts was greater than to other categories. Our data provide direct support for the role of human medial temporal regions in the representation of different categories of visual stimuli.
... Humans rapidly and accurately interpret visual scenes from their surrounding, an ability that is critical to normal functioning. One facet of visual perception of objects is view-invariant object recognition, which involves detection and identification of objects while discounting changes in low-level image statistics [Gross, 1994;Miyashita, 1993;Rolls, 2000;Orban, 2008;DiCarlo and Cox, 2007;. Visual perception of objects involves estimating a variety of other properties besides an object's category or identity, such as position, size, pose, lighting, occlusion, clutter, non-rigid deformation, and many other factors of the object that are normally discarded during invariant object recognition but are essential for defining scenes [Edelman, 1999;Koenderink and van Doorn, 19791. ...
... A framing hypothesis ( Fig. 1.3a) for how the brain achieves visual perception is that the ventral visual stream successively transforms and encodes low-level pixel-like patterns of neural responses into completely novel patterns of IT population neural responses that more explicitly represent high-level image content (e.g., object identity or category; for reviews, see [Gross, 1994;Miyashita, 1993;Rolls, 2000;Orban, 2008;DiCarlo and Cox, 2007;DiCarlo et al., 20121) and that the neural responses are decoded by the downstream areas to solve various tasks of visual perception [Miyashita, 1993;Freedman et al., 2003]. For example, the initial image-evoked IT neural population responses (100 ms latency) can directly support robust invariant visual object categorization and identification [Hung et al., 2005c;Li et al., 2006; Rust and DiCarlo, 2010], and IT population responses are far more useful for such tasks than are earlier ventral stream representations [Rust and DiCarlo, 2010;Freiwald and Tsao, 2010] or non-ventral stream representations [Lehky and Sereno, 2007]. ...
... Humans rapidly and accurately process visual scenes from their environment, an ability that is critical to normal functioning. One facet of scene understanding is [Tanaka, 1996;Logothetis and Sheinberg, 1996; Gross, 1994] that encode image content (e.g., object identity and category) increasingly explicitly in successive cortical areas [Vogels and Orban, 1994;DiCarlo and Cox, 2007;. For example, neurons in the lowest area, V1, are well-described by Gabor-like edge detectors [Carandini et al., 2005a], though the VI population does not show robust tolerance to complex image transformations . ...
Visual perception of objects is a computationally challenging problem and fundamental to human well-being. Extensive previous research has revealed that the inferior temporal cortex (IT), a high-level visual area, is involved in various aspects of visual perception. Yet, little is known about: how IT neural responses to objects support human perception of the objects; and how IT responses are produced from retinal images of objects. The goal of this research is to tackle these two related questions and find out explicit, quantitative mechanisms that describe human core visual perception of objects, a remarkable ability achieved with brief (
... The notion that the cerebral cortex is divided into functionally distinct cortices now known to be responsible for capacities such as touch (somatosensory cortex), movement (motor cortex), and vision (visual cortex), was first proposed by Franz Joseph Gall in 1810. [63] Evidence for functionally distinct areas of the brain (and, specifically, of the cerebral cortex) mounted throughout the 19th century with discoveries by Paul Broca of the language center (1861), and Gustav Fritsch and Edouard Hitzig of the motor cortex (1871). [63][64] Based on selective damage to parts of the brain and the functional effects of the resulting lesions, David Ferrier proposed that visual function was localized to the parietal lobe of the brain in 1876. ...
... [63] Evidence for functionally distinct areas of the brain (and, specifically, of the cerebral cortex) mounted throughout the 19th century with discoveries by Paul Broca of the language center (1861), and Gustav Fritsch and Edouard Hitzig of the motor cortex (1871). [63][64] Based on selective damage to parts of the brain and the functional effects of the resulting lesions, David Ferrier proposed that visual function was localized to the parietal lobe of the brain in 1876. [64] In 1881, Hermann Munk more accurately located vision in the occipital lobe, where the primary visual cortex is now known to be. ...
Mystery of extra-spectral magenta created wonder, and that wonder if blind see IR beyond rainbow, was the basis of desire to understand visual touch., which adds 50 pages to 130 page edition. John J Stapleton d/b/a StapleVision LLC staplevision@gmail.com 1 trans·duc·er a device that converts variations in a physical quantity, such as pressure or brightness, into an electrical signal, or vice versa, for example light photons→e→IR photons→ thermal/tactile cross-over 2 since the definition of unblind dates back to 1607 numerous ideas and schemes to give or restore sight to the blind have been in the mind of man beyond biblical miracles. VT is innate and natural, not supernatural. Unblind is a verb; an action word demands action. Unblind \Un*blind"\, v. t. [1st pref. un-+ blind] .
... The temporal lobe saw an accelerated atrophy and FA reduction that was not symmetrical, with more profound changes in the left hemisphere. This is of interest as the inferior temporal cortex is responsible for processing visual information from the occipital cortex [98]. The superior temporal cortex is involved in visual spatial-based processing and object-centered spatial orientation [99]. ...
Age-related macular degeneration (AMD) has recently been linked to cognitive impairment. We hypothesized that AMD modifies the brain aging trajectory, and we conducted a longitudinal diffusion MRI study on 40 participants (20 with AMD and 20 controls) to reveal the location, extent, and dynamics of AMD-related brain changes. Voxel-based analyses at the first visit identified reduced volume in AMD participants in the cuneate gyrus, associated with vision, and the temporal and bilateral cingulate gyrus, linked to higher cognition and memory. The second visit occurred 2 years after the first and revealed that AMD participants had reduced cingulate and superior frontal gyrus volumes, as well as lower fractional anisotropy (FA) for the bilateral occipital lobe, including the visual and the superior frontal cortex. We detected faster rates of volume and FA reduction in AMD participants in the left temporal cortex. We identified inter-lingual and lingual–cerebellar connections as important differentiators in AMD participants. Bundle analyses revealed that the lingual gyrus had a lower streamline length in the AMD participants at the first visit, indicating a connection between retinal and brain health. FA differences in select inter-lingual and lingual cerebellar bundles at the second visit showed downstream effects of vision loss. Our analyses revealed widespread changes in AMD participants, beyond brain networks directly involved in vision processing.
... Object detection and recognition are fundamental components of primate vision, and a substantial number of visual cortical areas are dedicated to processing visual objects [1][2][3][4][5] . However, vision does not occur in complete isolation of behavior, and an element of visual object processing in the brain must facilitate active orienting in association with objects, whether to avoid threats 6 or to foveate and further process behaviorally-relevant items. ...
Primate superior colliculus (SC) neurons exhibit visual feature tuning properties and are implicated in a subcortical network hypothesized to mediate fast threat and/or conspecific detection. However, the mechanisms through which SC neurons contribute to peripheral object detection, for supporting rapid orienting responses, remain unclear. Here we explored whether, and how quickly, SC neurons detect real-life object stimuli. We presented experimentally-controlled gray-scale images of seven different object categories, and their corresponding luminance- and spectral-matched image controls, within the extrafoveal response fields of SC neurons. We found that all of our functionally-identified SC neuron types preferentially detected real-life objects even in their very first stimulus-evoked visual bursts. Intriguingly, even visually-responsive motor-related neurons exhibited such robust early object detection. We further identified spatial frequency information in visual images as an important, but not exhaustive, source for the earliest (within 100 ms) but not for the late (after 100 ms) component of object detection by SC neurons. Our results demonstrate rapid and robust detection of extrafoveal visual objects by the SC. Besides supporting recent evidence that even SC saccade-related motor bursts can preferentially represent visual objects, these results reveal a plausible mechanism through which rapid orienting responses to extrafoveal visual objects can be mediated.
... Complexity in visual and other high order association areas is conferred by more influences through projections from other structures, including the thalamus (e.g., Galuske et al., 2000;da Costa and Martin, 2010), which activate monosynaptically not only layer 4 but also the deep layers, at least in rats (Constantinople and Bruno, 2013). In primates, the most anterior inferior temporal visual areas combine a broad map of the visual field with visual memory (e.g., Gross, 1994). Moreover, the "canonical" influence of projections on the cortical column, described to innervate layer 4, then the supragranular layers and then the infragranular layers in visual cortex (reviewed in Douglas and Martin, 2004), shows a different sequence when the monkey is required to recall paired associations from memory (Miyashita, 2022). ...
The idea of columns as an organizing cortical unit emerged from physiologic studies in the sensory systems. Connectional studies and molecular markers pointed to widespread presence of modular label that necessitated revision of the classical concept of columns. The general principle of cortical systematic variation in laminar structure is at the core of cortical organization. Systematic variation can be traced to the phylogenetically ancient limbic cortices, which have the simplest laminar structure, and continues through eulaminate cortices that show sequential elaboration of their six layers. Connections are governed by relational rules, whereby columns or modules with a vertical organization represent the feedforward mode of communication from earlier- to later processing cortices. Conversely, feedback connections are laminar-based and connect later- with earlier processing areas; both patterns are established in development. Based on studies in primates, the columnar/modular pattern of communication appears to be newer in evolution, while the broadly based laminar pattern represents an older system. The graded variation of cortices entails a rich variety of patterns of connections into modules, layers, and mixed arrangements as the laminar and modular patterns of communication intersect in the cortex. This framework suggests an ordered architecture poised to facilitate seamless recruitment of areas in behavior, in patterns that are affected in diseases of developmental origin.
... Traditionally, researchers have used intuition [10] or limited theoretical frameworks to choose a fixed set of stimuli, i.e., simple images, such as circles and rings for studying lateral geniculate nucleus cells, oriented bars for V1 neurons, hyperbolic gratings for V2 neurons [14], curved shapes for V4 neurons [23], or select categories such as faces for inferotemporal cortex neurons [7]. The desired property of these stimuli is their ability to drive neuronal activity. ...
Recently, optimization has become an emerging tool for neuroscientists to study neural code. In the visual system, neurons respond to images with graded and noisy responses. Image patterns eliciting highest responses are diagnostic of the coding content of the neuron. To find these patterns, we have used black-box optimizers to search a 4096d image space, leading to the evolution of images that maximize neuronal responses. Although genetic algorithm (GA) has been commonly used, there haven't been any systematic investigations to reveal the best performing optimizer or the underlying principles necessary to improve them. Here, we conducted a large scale in silico benchmark of optimizers for activation maximization and found that Covariance Matrix Adaptation (CMA) excelled in its achieved activation. We compared CMA against GA and found that CMA surpassed the maximal activation of GA by 66% in silico and 44% in vivo. We analyzed the structure of Evolution trajectories and found that the key to success was not covariance matrix adaptation, but local search towards informative dimensions and an effective step size decay. Guided by these principles and the geometry of the image manifold, we developed SphereCMA optimizer which competed well against CMA, proving the validity of the identified principles. Code available at https://github.com/Animadversio/ActMax-Optimizer-Dev
... The temporal cortex can be coarsely divided into four sub-regions: medial temporal cortex (MTC), superior temporal gyrus (STG), superior temporal sulcus (STS) and inferotemporal (IT) cortex (see (Gross, 1994) for a review). In this review, we are focusing on the STS and IT, as the MTC and STG have yet to evidence support for attentional control. ...
Attention is an indispensable component of active vision. Contrary to the widely accepted notion that temporal cortex processing primarily focusses on passive object recognition, a series of very recent studies emphasize the role of temporal cortex structures, specifically the superior temporal sulcus (STS) and inferotemporal (IT) cortex, in guiding attention and implementing cognitive programs relevant for behavioral tasks. The goal of this theoretical paper is to advance the hypothesis that the temporal cortex attention network (TAN) entails necessary components to actively participate in attentional control in a flexible task-dependent manner. First, we will briefly discuss the general architecture of the temporal cortex with a focus on the STS and IT cortex of monkeys and their modulation with attention. Then we will review evidence from behavioral and neurophysiological studies that supportsupport their guidance of attention in the presence of cognitive control signals. Next, we propose a mechanistic framework for executive control of attention in the temporal cortex. Finally, we summarize the role of temporal cortex in implementing cognitive programs and discuss how they contribute to the dynamic nature of visual attention to ensure flexible behavior.
... The inferior and middle temporal gyri are mainly associated with visual perception and multimodal sensory integration (144,145) but also emotional face processing (146). Damage to these regions has been related to deficits in tasks requiring visual discrimination and recognition (147). The activation of these areas seems intuitive given that half of our studies involved viewing faces or videos, and half involved listening to anger-eliciting scripts or audiotapes. ...
Background: While reactive aggression (in response to a perceived threat or provocation) is part of humans' adaptive behavioral repertoire, it can violate social and legal norms. Understanding brain function in individuals with high levels of reactive aggression as they process anger- and aggression-eliciting stimuli is critical for refining interventions. Three neurobiological models of reactive aggression - the limbic hyperactivity, prefrontal hypoactivity, and dysregulated limbic-prefrontal connectivity models - have been proposed. However, these models are based on neuroimaging studies involving mainly healthy individuals, leaving it unclear which model best describes brain function in aggression-prone individuals.
Methods: We conducted a systematic literature search (PubMed and Psycinfo) and Multilevel Kernel Density meta-analysis (MKDA) of nine functional magnetic resonance imaging (fMRI) studies of brain responses to tasks putatively eliciting anger and aggression in aggression-prone individuals alone, and relative to healthy controls.
Results: Aggression-prone individuals exhibited greater activity during reactive aggression relative to baseline in the superior temporal gyrus and in regions comprising the cognitive control and default mode networks (right posterior cingulate cortex, precentral gyrus, precuneus, right inferior frontal gyrus). Compared to healthy controls, aggression-prone individuals exhibited increased activity in limbic regions (left hippocampus, left amygdala, left parahippocampal gyrus) and temporal regions (superior, middle, inferior temporal gyrus), and reduced activity in occipital regions (left occipital cortex, left calcarine cortex).
Conclusions: These findings lend support to the limbic hyperactivity model and further indicate altered temporal and occipital activity in anger- and aggression-eliciting situations that involve face and speech processing.
... P rimates have a dedicated visual system to process faces 1,2 . Earlier work in monkeys have revealed face-selective neurons in the inferotemporal (IT) cortex (see 3 for a historical overview), which has been later verified in human intracranial recordings 4 . In particular, while classically investigated for their roles in long-term memory 5 , the human amygdala and hippocampus have been associated with various roles in face perception [6][7][8][9] . ...
Faces are salient social stimuli that attract a stereotypical pattern of eye movement. The human amygdala and hippocampus are involved in various aspects of face processing; however, it remains unclear how they encode the content of fixations when viewing faces. To answer this question, we employed single-neuron recordings with simultaneous eye tracking when participants viewed natural face stimuli. We found a class of neurons in the human amygdala and hippocampus that encoded salient facial features such as the eyes and mouth. With a control experiment using non-face stimuli, we further showed that feature selectivity was specific to faces. We also found another population of neurons that differentiated saccades to the eyes vs. the mouth. Population decoding confirmed our results and further revealed the temporal dynamics of face feature coding. Interestingly, we found that the amygdala and hippocampus played different roles in encoding facial features. Lastly, we revealed two functional roles of feature-selective neurons: 1) they encoded the salient region for face recognition, and 2) they were related to perceived social trait judgments. Together, our results link eye movement with neural face processing and provide important mechanistic insights for human face perception.
... The temporal cortex can be coarsely divided into four sub-regions: medial temporal cortex (MTC), superior temporal gyrus (STG), superior temporal sulcus (STS) and inferotemporal (IT) cortex (see (Gross, 1994) for a review). In this review, we are focusing on the STS and IT, as the MTC and STG have yet to evidence support for attentional control. ...
Attention is an indispensable component of active vision. Contrary to the widely accepted notion that temporal cortex processing primarily focusses on passive object recognition, a series of very recent studies emphasize the role of temporal cortex structures, specifically the superior temporal sulcus (STS) and inferotemporal (IT) cortex, in guiding attention and implementing cognitive programs relevant for behavioral tasks. The goal of this theoretical paper is to advance the hypothesis that the temporal cortex attention network (TAN) entails necessary components to actively participate in attentional control in a flexible task-dependent manner. First, we will briefly discuss the general architecture of the temporal cortex with a focus on the STS and IT cortex of monkeys and their modulation with attention. Then we will review evidence from behavioral and neurophysiological studies that support their guidance of attention in the presence of cognitive control signals. Next, we propose a mechanistic framework for executive control of attention in the temporal cortex. Finally, we summarize the role of temporal cortex in implementing cognitive programs and discuss how they contribute to the dynamic nature of visual attention to ensure flexible behavior.
... A study in macaques suggested the role of the middle temporal gyrus in visual connection associated with object vision. The same study showed ablation of this area causes a learning deficit in visual object discrimination and recognition (Gross, 1994). In another study, higher activation of the middle temporal gyrus was linked to perceiving facial attractiveness and expression (Vartanian et al., 2013). ...
Although visual processing impairments have been explored in schizophrenia (SZ), their underlying neurobiology of the visual processing impairments has not been widely studied. Also, while some research has hinted at differences in information transfer and flow in SZ, there are few investigations of the dynamics of functional connectivity within visual networks. In this study, we analyzed resting-state fMRI data of the visual sensory network (VSN) in 160 healthy control (HC) subjects and 151 SZ subjects. We estimated 9 independent components within the VSN. Then, we calculated the dynamic functional network connectivity (dFNC) using the Pearson correlation. Next, using k-means clustering, we partitioned the dFNCs into five distinct states, and then we calculated the portion of time each subject spent in each state, which we termed the occupancy rate (OCR). Using OCR, we compared HC with SZ subjects and investigated the link between OCR and visual learning in SZ subjects. Besides, we compared the VSN functional connectivity of SZ and HC subjects in each state. We found that this network is indeed highly dynamic. Each state represents a unique connectivity pattern of fluctuations in VSN FNC, and all states showed significant disruption in SZ. Overall, HC showed stronger connectivity within the VSN in states. SZ subjects spent more time in a state in which the connectivity between the middle temporal gyrus and other regions of VNS is highly negative. Besides, OCR in a state with strong positive connectivity between the middle temporal gyrus and other regions correlated significantly with visual learning scores in SZ.
... A study in macaques suggested the role of the middle temporal gyrus in visual connection associated with object vision. The same study showed ablation of this area causes a learning deficit in visual object discrimination and recognition (Gross, 1994). In another study, higher activation of the middle temporal gyrus was linked to perceiving facial attractiveness and expression (Vartanian et al., 2013). ...
Although visual processing impairments have been explored in schizophrenia (SZ), their underlying neurobiology of the visual processing impairments has not been widely studied. Also, while some research has hinted at differences in information transfer and flow in SZ, there are few investigations of the dynamics of functional connectivity within visual networks. In this study, we analyzed resting-state fMRI data of the visual sensory network (VSN) in 160 healthy control (HC) subjects and 151 SZ subjects. We estimated 9 independent components within the VSN. Then, we calculated the dynamic functional network connectivity (dFNC) using the Pearson correlation. Next, using k-means clustering, we partitioned the dFNCs into five distinct states, and then we calculated the portion of time each subject spent in each state, that we termed the occupancy rate (OCR). Using OCR, we compared HC with SZ subjects and investigated the link between OCR and visual learning in SZ subjects. Besides, we compared the VSN functional connectivity of SZ and HC subjects in each state. We found that this network is indeed highly dynamic. Each state represents a unique connectivity pattern of fluctuations in VSN FNC, and all states showed significant disruption in SZ. Overall, HC showed stronger connectivity within the VSN in states. SZ subjects spent more time in a state in which the connectivity between the middle temporal gyrus and other regions of VNS is highly negative. Besides, OCR in a state with strong positive connectivity between middle temporal gyrus and other regions correlated significantly with visual learning scores in SZ.
... We will discuss the next three areas together because they are all related to the visual function of the brain. Anatomic, ablation, and physiological evidence all suggest that the neuronal mechanisms that connect vision and memory in primates are located within the inferior temporal cortex, which consists of the middle temporal gyrus and the inferior temporal gyrus anatomically [43]- [45]. The fusiform is involved in both detection and identification of faces [46]. ...
Resting-state fMRI studies have suggested that autism spectrum disorder (ASD) is associated with aberrant dynamic changes. However, existing research either has difficulty showing the brain’s dynamic characteristics or cannot obtain stable results. We examined the ‘two-group cross-location hidden Markov model’ of each region of interest (ROI) to identify possible pathogenic features of ASD. Specifically, we selected resting-state fMRI data with complete scales and good quality from Autism Brain Imaging Data Exchange (ABIDEI). Eligible data included 145 ASD and 157 control (CON). Two groups of subjects were separated to train Hidden Markov models representing respective populations. Then, we used each model to estimate the likelihood values of all participants. Using the likelihood value as features, we tested the significant differences of 200 ROIs and finally identified ROIs with common significant differences in the two types of models. Additionally, we investigated the relationship between likelihood values of significantly different ROIs and clinical scales. some ROIs were negatively correlated with the Autism Diagnostic Observation Schedule and positively correlated with full IQ. Finally, we constructed a support vector machine to classify ASD and CON. Overall, our findings suggested that the abnormal areas in the frontopolar area, orbitofrontal area, inferior temporal gyrus, middle temporal gyrus and fusiform gyrus are prominent features of ASD and are closely related to clinical functional decline. The average accuracy rate reached 74.9% after ten cross-validations. This ‘two-group cross-localized Hidden Markov Model’ provides a robust and powerful framework for understanding the dysfunctional brain architecture of ASD.
... Bilateral lesions of the inferotemporal cortex profoundly impair object recognition. However, it has been known since the work of Brown & Schaeffer ( 1888) and reconfirmed (Gross, 1992) that visual fields, visual acuity and elemental visual discriminations remain intact following bilateral ablations of the inferotemporal cortices. Corresponding findings have been confirmed in braindamaged human subjects (Damasio, 1999). ...
... Here, we not only confirmed the strong effect of image scrambling on SUA, MUA, and high-gamma responses in LOC, but we also revealed significant response differences for intact shapes, i.e., shape selectivity, at the level of single neurons, as previously shown in the macaque ITC [36,37]. A bilateral lesion of LOC produces a profound deficit in shape recognition [38][39][40], similar to ITC lesions in monkeys [41][42][43][44][45], and transcranial magnetic stimulation over LOC also impairs shape discrimination [46,47]. Our data support the notion that these deficits arise from a loss of shape-selective neurons in LOC. ...
The human lateral occipital complex (LOC) is more strongly activated by images of objects compared to scrambled controls, but detailed information at the neuronal level is currently lacking. We recorded with microelectrode arrays in the LOC of 2 patients and obtained highly selective single-unit, multi-unit, and high-gamma responses to images of objects. Contrary to predictions derived from functional imaging studies, all neuronal properties indicated that the posterior subsector of LOC we recorded from occupies an unexpectedly high position in the hierarchy of visual areas. Notably, the response latencies of LOC neurons were long, the shape selectivity was spatially clustered, LOC receptive fields (RFs) were large and bilateral, and a number of LOC neurons exhibited three-dimensional (3D)-structure selectivity (a preference for convex or concave stimuli), which are all properties typical of end-stage ventral stream areas. Thus, our results challenge prevailing ideas about the position of the more posterior subsector of LOC in the hierarchy of visual areas.
... Towards the end of this section, it should be mentioned that in the late 19th century some progress was made in memory function, as French psychologist Théodule Ribot distinguished anterograde from retrograde amnesia stressing that recent memories are more vulnerable to brain damage than remote ones; also, Wernicke and Russian psychiatrist Sergei Korsakoff described the amnesic syndrome that took their name [40]. Nevertheless, some evidence connecting memory with TL, obtained in the context of Schafer's and his American colleague Sanger Brown's examination study of hearing after TL excision in a monkey [41], and particularly with the hippocampus, produced by the Russian's neurologist Vladimir Bekhterev's lesion-detection study in a patient with amnesia, were rapidly forgotten [42]. ...
... Four seed regions 188 of interest (ROI) for the articulatory system were chosen a priori, based on activation peaks 189 reported previously (Brown et al. 2008 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 212 1, A). The inferior temporal gyrus was not included since this area is more closely involved in 213 visual rather than auditory processing (Gross 1994). (Stephens, Silbert, & Hasson, 2010). ...
Whether auditory processing of speech relies on reference to the articulatory motor information of speaker remains elusive. Here, we addressed this issue under a two-brain framework. Functional magnetic resonance imaging was applied to record the brain activities of speakers when telling real-life stories and later of listeners when listening to the audio recordings of these stories. Based on between-brain seed-to-voxel correlation analyses, we revealed that neural dynamics in listeners' auditory temporal cortex are temporally coupled with the dynamics in the speaker's larynx/phonation area. Moreover, the coupling response in listener's left auditory temporal cortex follows the hierarchical organization for speech processing, with response lags in A1+, STG/STS, and MTG increasing linearly. Further, listeners showing greater coupling responses understand the speech better. When comprehension fails, such interbrain auditory-articulation coupling vanishes substantially. These findings suggest that a listener's auditory system and a speaker's articulatory system are inherently aligned during naturalistic verbal interaction, and such alignment is associated with high-level information transfer from the speaker to the listener. Our study provides reliable evidence supporting that references to the articulatory motor information of speaker facilitate speech comprehension under a naturalistic scene.
... Here, we not only confirmed the strong effect of image 282 scrambling on SUA, MUA and high-gamma responses in LOC, but we also revealed significant response 283 differences for intact shapes, i.e. shape selectivity, at the level of single neurons, as previously shown 284 in the macaque ITC ( Sheinberg, 1996, Tanaka, 1996). A bilateral lesion of LOC produces 285 a profound deficit in shape recognition ( Goodale et al., 1991, James et al., 2003, Westwood and 286 Goodale, 2011), similar to ITC lesions in monkeys (Cowey and Gross, 1970, Britten et al., 1992, Dean, 287 1976, Gross, 1994, Dean, 1979 Kajikawa and Schroeder, 2011). Although our data do not allow us to fully resolve this controversy, it 308 should be noted that our spatially-selective recordings were obtained during an active fixation task, 309 where no influence of anesthetics was possible, in contrast to the Kajikawa and Schroeder study. ...
The human lateral occipital complex (LOC) is more strongly activated by images of objects compared to scrambled controls, but detailed information at the neuronal level is currently lacking. We recorded with microelectrode arrays in the LOC of two patients, and obtained highly selective single-unit, multi-unit and high-gamma responses to images of objects. Contrary to predictions derived from functional imaging studies, all neuronal properties indicated that the subsector of LOC we recorded from occupies an unexpectedly high position in the hierarchy of visual areas. Notably, the response latencies of LOC neurons were long, the shape selectivity was spatially clustered, LOC receptive fields were large and bilateral, and a number of LOC neurons exhibited 3D-structure selectivity (a preference for convex or concave stimuli), which are all properties typical of end-stage ventral stream areas. Thus, our results challenge prevailing ideas about the position of the LOC in the hierarchy of visual areas.
... Visual system is one of the most widely and intensely studied sensory systems, as well as the most complex sensory nervous system; however the underlying visual mechanism is yet to be elucidated (Jessell Thomas et al. 2000;Rieke et al. 1997;Yan et al. 2016; Barranca et al. 2014). The surrounding visual information is processed in the retina, lateral geniculate nucleus, visual cortex, and other regions of the central nervous system (Schiller 1986;Gross 1994;Qiu et al. 2016). A large number of biological experiments are focused on the lateral geniculate and visual cortex of the visual system. ...
Advances in neurobiology suggest that neuronal response of the primary visual cortex to natural stimuli may be attributed to sparse approximation of images, encoding stimuli to activate specific neurons although the underlying mechanisms are still unclear. The responses of retinal ganglion cells (RGCs) to natural and random checkerboard stimuli were simulated using fast independent component analysis. The neuronal response to stimuli was measured using kurtosis and Treves–Rolls sparseness, and the kurtosis, lifetime and population sparseness were analyzed. RGCs exhibited significant lifetime sparseness in response to natural stimuli and random checkerboard stimuli. About 65 and 72% of RGCs do not fire all the time in response to natural and random checkerboard stimuli, respectively. Both kurtosis of single neurons and lifetime response of single neurons values were larger in the case of natural than in random checkerboard stimuli. The population of RGCs fire much less in response to random checkerboard stimuli than natural stimuli. However, kurtosis of population sparseness and population response of the entire neurons were larger with natural than random checkerboard stimuli. RGCs fire more sparsely in response to natural stimuli. Individual neurons fire at a low rate, while the occasional “burst” of neuronal population transmits information efficiently.
... RAVLT-7 was positively correlated with the WDs in the inferior temporal gyrus. The inferior temporal gyrus contributes to encoding and storage of visual information of an object, possibly through its anatomical connections with the hippocampus and the parahippocampal gyrus (Gross 1994(Gross , 2008Kirchhoff et al. 2000). It is well-established that the hippocampus plays a pivotal role in establishing long-term episodic memory, evidenced by neural activation in this region during memory retrieval (Squire and Zola-Morgan 1991;Davachi et al. 2003). ...
In previous studies, resting-state functional connectivity (FC) metrics of specific brain regions or networks based on prior hypotheses have been correlated with cognitive performance. Without constraining our analyses to specific regions or networks, we employed whole-brain voxel-based weighted degree (WD), a measure of local FC strength, to be correlated with three commonly used neuropsychological assessments of language, executive function and memory retrieval in both positive and negative directions in 67 cognitively healthy elderly adults. We also divided voxel-based WD into short-ranged and long-ranged WDs to evaluate the influence of FC distance on the WD-cognition relationship, and performed three validation tests. Our results showed that for language and executive function tests, positive WD correlates were located in the frontal and temporal cortices, and negative WD correlates in the precuneus and occipital cortices; for memory retrieval, positive WD correlates were located in the inferior temporal cortices, and negative WD correlates in the anterior cingulate cortices and supplementary motor areas. An FC-distance-dependent effect was also observed, with the short-ranged WD correlates of language and executive function tests located in the medial brain regions and the long-ranged WD correlates in the lateral regions. Our findings suggest that inter-individual differences in FC at rest are predictive of cognitive ability in the elderly adults. Moreover, the distinct patterns of positive and negative WD correlates of cognitive performance recapitulate the dichotomy between task-activated and task-deactivated neural systems, implying that a competition between distinct neural systems on functional network topology may have cognitive relevance.
... Converging evidence from behavioral, functional, and lesional data has identified a subset of cortical regions, biased towards the right hemisphere, that are believed to form a distributed network for face perception [1][2][3][4]. Current insights into the neural basis of face perception are derived from studies of brain-lesions [5][6][7][8][9][10][11][12] and single neuron recordings [13][14][15] in the monkey inferotemporal cortex (IT) (for review see [16,17]). More recently, electrophysiological studies in non-human primates have identified as many as six, widely distributed face-selective neuronal clusters[18]-from the superior temporal sulcus (STS; upper and lower) to anterior IT [19][20][21][22][23]. ...
Prevailing theories suggests that cortical regions responsible for face perception operate in a serial, feed-forward fashion. Here, we utilize invasive human electrophysiology to evaluate serial models of face-processing via measurements of cortical activation, functional connectivity, and cortico-cortical evoked potentials. We find that task-dependent changes in functional connectivity between face-selective regions in the inferior occipital (f-IOG) and fusiform gyrus (f-FG) are bidirectional, not feed-forward, and emerge following feed-forward input from early visual cortex (EVC) to both of these regions. Cortico-cortical evoked potentials similarly reveal independent signal propagations between EVC and both f-IOG and f-FG. These findings are incompatible with serial models, and support a parallel, distributed network underpinning face perception in humans.
... It should be noted that the hippocampus of the elephant is not larger than would be expected for its brain mass (Patzke et al. 2014b(Patzke et al. , 2015, thus the rotation and position of the amygdaloid complex is not related to any incorrectly assumed expansion of the hippocampus (Hakeem et al. 2005). A somewhat similar, but not as exaggerated, rotation of the amygdaloid complex is observed in primates, presumably associated with the expanded temporal lobe of primates associated with increased cortical territory devoted to visual processing (Gross 1994). Despite this rotation, the loss of certain nuclei and the expansion of certain nuclei, the internal topological relationships of the amygdaloid nuclei are not drastically different in the elephant when compared to other mammals. ...
Here we describe the nuclear organization of the African elephant amygdaloid complex using Nissl, myelin, and a range of immunohistochemical stains. The African elephant is thought to exhibit many affect-laden and social-empathic behaviours; however, to date the amygdaloid complex, which is the generator of emotional states of the brain is yet to be fully explored in the elephants. For the most part, the amygdaloid complex of the African elephant is similar to that observed in other mammals in terms of the presence of nuclei and their topological relationships; however, we did observe several specific differences in amygdaloid organization. The elephant amygdala has undergone rotation in both the coronal and sagittal planes, seemingly associated with the expansion of the temporal lobe. Numerous scalloped cell clusters, termed glomeruli, forming the intermediate nuclei of the basal, accessory basal and central nuclear groups, were occupied by structures immunopositive to doublecortin. The nuclei typically associated with the accessory olfactory system (posterior cortical nucleus and medial nuclear complex) were absent from the elephant amygdala. The anterior cortical nucleus is very large and appears to be comprised of two subdivisions. The lateral nuclear complex is expanded and has two novel subdivisions. The amygdalohippocampal area appears relatively enlarged. The numerous shared and derived characters make the elephant amygdaloid complex very unusual and unique amongst mammals, but the derived characters appear to relate to observed elephant affect-laden behaviours.
... Functional characterization of the left PMd ventral module showed a behavioral pattern dominated by visual and language-related functions. Accordingly, functional connectivity across MACM and RSFC showed that the ventral left PMd is functionally coupled with Broca's area and TE areas assigned to the ventral processing stream supporting object recognition (Gross 1994). When examining the functional profile of the left PMd ventral module and its spatial correspondence with the right PMd premotor eye-field, it appeared that the left PMd ventral module conceptually overlapped with the left premotor eye-field. ...
Despite the common conception of the dorsal premotor cortex (PMd) as a single brain region, its diverse connectivity profiles and behavioral heterogeneity argue for a differentiated organization of the PMd. A previous study revealed that the right PMd is characterized by a rostro-caudal and a ventro-dorsal distinction dividing it into five subregions: rostral, central, caudal, ventral and dorsal. The present study assessed whether a similar organization is present in the left hemisphere, by capitalizing on a multimodal data-driven approach combining connectivity-based parcellation (CBP) based on meta-analytic modeling, resting-state functional connectivity, and probabilistic diffusion tractography. The resulting PMd modules were then characterized based on multimodal functional connectivity and a quantitative analysis of associated behavioral functions. Analyzing the clusters consistent across all modalities revealed an organization of the left PMd that mirrored its right counterpart to a large degree. Again, caudal, central and rostral modules reflected a cognitive-motor gradient and a premotor eye-field was found in the ventral part of the left PMd. In addition, a distinct module linked to abstract cognitive functions was observed in the rostro-ventral left PMd across all CBP modalities, implying greater differentiation of higher cognitive functions for the left than the right PMd.
... Though the brain regions showing a preference for unique entities were found to be multimodal in previous literature (Binder and Desai, 2011;Ghazanfar and Schroeder, 2006;Lambon Ralph, 2014;Visser et al., 2010), visual input might play a critical role in differentiating unique entities from their common counterparts in these regions. The possibility that stronger activity to unique entities might reflect the retrieval of visual knowledge is particularly relevant for regions in temporal cortex: the bilateral ATLs are traditionally considered to be the end point of the ventral visual pathway (Gross, 1994;Gross et al., 1969;Kravitz et al., 2013). Studies on macaques and humans have found that the right ATL differentiates between individual faces (Freiwald and Tsao, 2010;Kriegeskorte et al., 2007; see Anzellotti and Caramazza, 2014 for a review), suggesting that it represents high-level visual information specific to individual entities. ...
Famous places and famous people are different from their common counterparts in that we have unique knowledge about individual items, including specific knowledge about their visual appearance and other sensory properties. Previous studies have shown that the processing of unique entities selectively activates a network of brain regions that includes the bilateral anterior temporal lobes (ATL), posterior cingulate cortex and adjacent medial precuneus (PCC/medPrec), medial prefrontal cortex (medPFC), and temporal-parietal junction (TPJ). The degree to which these regions represent visual properties associated with famous people/places is unknown. Here we compared fMRI responses in congenitally and sighted individuals to test whether visual experience contributes to the development of unique-entity responses in these regions. Names of unique entities (famous places, famous people) and generic items (daily scenes such as “bridge”, face parts) were presented aurally to 13 congenitally blind and 16 sighted participants. Sighted participants additionally viewed corresponding photographs. We found that bilateral PCC/medPrec, medPFC, left TPJ, left ATL and right superior frontal gyrus were more strongly activated by pictures of unique entities compared to generic items. Importantly, all regions showed similar selectivity for unique entities in both groups when only names were presented. Furthermore, resting-state functional connectivity analysis revealed that these regions were tightly interconnected in both groups. Together, these results provide evidence for a visually-independent brain network underlying unique entity processing.
... Occipito-temporal regions, including inferior temporal, lingual and fusiform gyri showed predominantly left hemisphere activation. Extensive activation of these regions has been reported in studies of selective attention to visual shape or form and performance on visual target detection tasks [5,10,20,21]. It seems reasonable to assume that the occipito-temporal activation observed in the present study re¯ects an increasing requirement for the detection and discrimination of visual cues across conditions. ...
... identified a neuron in inferior temporal (IT) cortex of a macaque monkey that selectively responded to images of hands. The results were so surprising that Gross (1994) later recounted how he was initially nervous to call the neuron a ''hand cell", and speculated that this work was largely ignored for a decade because researchers didn't believe the findings. Subsequently there have been dozens of studies reporting similar findings, and the observation that some neurons in cortex and hippocampus respond to high-level perceptual information in a highly selective manner is no longer in doubt (for a detailed review of the neuroscience, see Bowers, 2009). ...
Why do some neurons in hippocampus and cortex respond to information in a highly selective manner? It has been hypothesized that neurons in hippocampus encode information in a highly selective manner in order to support fast learning without catastrophic interference, and that neurons in cortex encode information in a highly selective manner in order to co-activate multiple items in short-term memory (STM) without suffering a superposition catastrophe. However, the latter hypothesis is at odds with the widespread view that neural coding in the cortex is highly distributed in order to support generalization. We report a series of simulations that characterize the conditions in which recurrent Parallel Distributed Processing (PDP) models of immediate serial can recall novel words. We found that these models learned localist codes when they succeeded in generalizing to novel words. That is, just as fast learning may explain selective coding in hippocampus, STM and generalization may help explain the existence of selective codes in cortex.
... Twenty-seven percent of the frontal lobe nodes had a lower nodal degree, including the superior frontal, caudal anterior, and middle cingulate affected predominantly in the left hemisphere. The inferior temporal and fusiform were affected in the left temporal lobe-areas of the brain that are responsible for identifying objects and face perception [Gross, 1994]. The nodes on the pericalcarine cortex (anatomical location of primary visual cortex [Bedny, 2011]) and lingual areas presented with a lower nodal degree in the left hemisphere occipital lobe. ...
In network analysis, the so-called "rich club" describes the core areas of the brain that are more densely interconnected among themselves than expected by chance, and has been identified as a fundamental aspect of the human brain connectome. This is the first in-depth diffusion imaging study to investigate the rich club along with other organizational changes in the brain's anatomical network in behavioral frontotemporal dementia (bvFTD), and a matched cohort with early-onset Alzheimer's disease (EOAD). Our study sheds light on how bvFTD and EOAD affect connectivity of white matter fiber pathways in the brain, revealing differences and commonalities in the connectome among the dementias. To analyze the breakdown in connectivity, we studied three groups: 20 bvFTD, 23 EOAD, and 37 healthy elderly controls. All participants were scanned with diffusion-weighted magnetic resonance imaging (MRI), and based on whole-brain probabilistic tractography and cortical parcellations, we analyzed the rich club of the brain's connectivity network. This revealed distinct patterns of disruption in both forms of dementia. In the connectome, we detected less disruption overall in EOAD than in bvFTD [false discovery rate (FDR) critical Pperm = 5.7 × 10(-3) , 10,000 permutations], with more involvement of richly interconnected areas of the brain (chi-squared P = 1.4 × 10(-4) )-predominantly posterior cognitive alterations. In bvFTD, we found a greater spread of disruption including the rich club (FDR critical Pperm = 6 × 10(-4) ), but especially more peripheral alterations (chi-squared P = 6.5 × 10(-3) ), particularly in medial frontal areas of the brain, in line with the known behavioral socioemotional deficits seen in these patients. Hum Brain Mapp, 2015. © 2015 The Authors. Human Brain Mapping Published by Wiley Periodicals, Inc.
... In order to understand neural mechanisms of object recognition, we have investigated representation of object images in inferotemporal (IT) cortex of macaque monkeys. This area of brain is essential for the recognition of objects by their visual images, and neurons in this area are known to respond to images of complex objects (Gross 1994;Gross et al. 1979;Desimone et al. 1984;Bruce et al. 1981 Tanaka et al. 1991). Although some of these neurons specifically respond to certain objects such as faces, many IT neurons also well respond to visual features that are less complex than object images (Desimone et al. 1984;Bruce et al. 1981;Perrett et al. 1982;Tanaka et al. 1991). ...
Optical imaging of intrinsic signals has extended our understanding of the functional organization of primary somatosensory cortex (SI) in primates. This chapter describes the findings which show that somatotopy, long a staple of somatosensory cortical functional organization, may not be as precise as the maps drawn from single and multiunit recordings. Optical maps of the tactile funneling illusion, which demonstrates a map of how tactile stimuli are perceived in SI rather than a map of skin topography, support the topographic representation in SI which is not a physical body map, but a perceptual map. Optical images of vibrotactile pressure, flutter, and vibration submodality domains overlaying the somatotopy reveal striking similarities and differences between other modality maps in somatosensory as revealed through electrophysiological methods and visual cortices as revealed through optical imaging methods. In an effort to extend these findings to functional MRI studies and somatic perception in humans, we compared in the same animal the maps acquired with high spatial resolution optical imaging in monkey SI with positive BOLD maps acquired at high filed (9.4T). We demonstrated that the positive BOLD fMRI maps were comparable to the fine scale OI maps in revealing both somatotopy and funneling. With the addition of high field human fMRI studies at 7 Tesla, this combination of approaches can investigate the relationship between somatotopic representation and sensory perception from the human to the modular domain and single unit level in primates. © Springer Science+Business Media, LLC 2010. All rights reserved.
... As detailed in the introduction, the processing of visual information is supposed to rely on two pathways. On the one hand, the ventral pathway, going from the occipital lobe through the temporal lobe is classically thought to mediate object recognition (Gross, 1994). Several studies have shown the influence of the intrinsic properties of an object of interest on the processing of single cells (Chelazzi et al., 1998). ...
Ce document tente de promouvoir, au travers de recherches passées et de propositions nouvelles, un cadre computationel pour l'étude de la cognition. En ce sens, la notion de calculs numériques distribués et adaptatifs est détaillée afin de mieux comprendre pourquoi nous pouvons prétendre à la légitimité dans les modèles numériques que nous concevons pour décrire la Biologie et le Vivant.
Considerable research has been devoted to understanding the fundamental organizing principles of the ventral visual pathway. A recent study revealed a series of 3-4 topographical maps arranged along the macaque inferotemporal (IT) cortex. The maps articulated a two-dimensional space based on the spikiness and animacy of visual objects, with "inanimate-spiky" and "inanimate-stubby" regions of the maps constituting two previously unidentified cortical networks. The goal of our study was to determine whether a similar functional organization might exist in human IT. To address this question, we presented the same object stimuli and images from "classic" object categories (bodies, faces, houses) to humans while recording fMRI activity at 7 Tesla. Contrasts designed to reveal the spikiness-animacy object space evoked extensive significant activation across human IT. However, unlike the macaque, we did not observe a clear sequence of complete maps, and selectivity for the spikiness-animacy space was deeply and mutually entangled with category-selectivity. Instead, we observed multiple new stimulus preferences in category-selective regions, including functional sub-structure related to object spikiness in scene-selective cortex. Taken together, these findings highlight spikiness as a promising organizing principle of human IT and provide new insights into the role of category-selective regions in visual object processing.
Temporal lobe is known to perform vital role in visual discrimination and identification of objects. Cresyl violet and Golgi studies of temporal region of Indian gray mongoose revealed diversity of neurons dispersed in six layers of the region. Pyramidal neurons were observed to outnumber the other four types of neurons in the temporal region supporting the specialization of this brain region as compared to primitive brains of monotremes and insectivores. Moreover, specialization of neurons provides better functioning and refining learning and predatory behavior of the animal.
Some images spontaneously change in appearance. A new study has found that these changes are reflected in high-level visual cortical areas before they become apparent in early sensory cortex. This suggests that visual information not only flows towards interpretative areas of our brain, but also in the reverse direction.
The frontal eye filed (FEF) is a relatively small frontal region that has been intensely studied. It received multiple definitions that help to locate it with some discrepancies between non-human primates and humans. The goal of this review is to provide an inter-species comparison of the location, extent, and boundaries of the FEF through the multiple anatomical and functional methodologies that has been used for its description as an oculomotor-associated area. We therefore propose a new orientation for using white matter fibers co-localizations between frontal structures to study their evolution and clarify the FEF homologies in primates.
Key Thinkers in Neuroscience provides insight into the life and work of some of the most significant minds that have shaped the field. Studies of the human brain have been varied and complex, and the field is rich in pioneers whose endeavours have broken new ground in neuroscience. Adopting a chronological and multi-disciplinary approach to each Key Thinker, the book highlights their extraordinary contributions to neuroscience. Beginning with Santiago Ramon y Cajal and finishing with the philosophers Patricia Churchland and Paul Churchland, this book provides a comprehensive look at the new ideas and discoveries that have shaped neuroscientific research and practice, and the people that have been invaluable to this field. This book will be an indispensable companion for all students of neuroscience and the history of psychology, as well as anyone interested in how we have built our knowledge of the brain.
Throughout history, researchers who examine the structure and function of the brain debate one another about how cortical areas are defined, as well as how these areas should be named. Different pieces of empirical evidence are used to define brain areas and it is important to preserve the accurate history of this evidence and the timeline of studies that lead to areal definitions that are either still used today or have been modified. As such, this paper traces the early history of a brain area located at the junction between the occipital and temporal lobes of the macaque known as TEO. This historical analysis leads to four main findings. First, even though Bonin and Bailey are credited with the definition of area TEO in 1947, they did not have the cytoarchitectonic evidence to support the distinction of TEO from adjacent areas. Second, the first evidence definitively separating area TEO from TE was actually based on connectivity as identified with strychnine neuronography by Petr et al. in 1949. Third, causal evidence from ablation studies conducted by Iwai and Mishkin (Experimental Neurology 25(4):585-594, 1969) supported this distinction by showing that TEO and TE were functionally distinct from one another. Fourth, researchers in the 1970s began referring to TEO as posterior inferotemporal (PIT) and TE as anterior inferotemporal (AIT), which is an important historical clarification as the PIT/AIT nomenclature is presently attributed to studies conducted more than a decade later. Altogether, this paper aims to preserve the historical origin of area TEO, as well as the empirical evidence that was used to originally differentiate this cortical expanse from surrounding areas.
Investigating the living brain, and in particular relating its activity to behavior is one of the most important challenges in neuroscience. Researchers use many different techniques to explore this relationship. Careful observation of patients with brain lesions or neuroimaging methods such as functional magnetic resonance imaging (fMRI), electroencephalography (EEG), or near infra-red spectroscopy (NIRS) are examples of procedures which allow researchers to make inferences about brain activity in a non-invasive way.
Saliency historically refers to the bottom-up visual properties of an object that automatically drive attention. It is an ordinal property that depends on the relative saliency of one object with respect to others in the scene. Simple examples are a red spot on a green background, a horizontal bar among vertical bars, or a sudden onset of motion. Researchers have introduced the idea of a saliency map, an abstract and featureless map of the ‘winners’ of attention competition, to model the dynamics of visual attention. The standard saliency map involves channels like color, orientation, size, shape, movement or unique onset. But how do complex stimuli, especially stimuli with social meaning such as faces, pop out and attract attention? Suppose you are attending a big party: your attention might be captured by someone in a fancy dress, someone looking at you, someone who is attractive, familiar, or distinctive in some way. This happens essentially automatically, and encompasses a huge number of different stimuli that are all competing for your attention. What determines which is the most salient, and how can we best measure this?
Recently, the Deep Convolutional Neural Networks (DCNN) have achieved state-of-the-art performances with many tasks in image and video analysis. However, it is a very challenging problem to devise a good DCNN model as there are so many choices to be made by a network designer, including the depth, the number of feature maps, interconnection patterns, window sizes for convolution and pooling layers, etc. These choices constitute a huge search space that makes it impractical to discover an optimal network structure with any systematic approaches. In this paper, we strive to develop a good DCNN model by borrowing biological guidance from the human visual cortex. By making an analogy between the proposed DCNN model and the human visual cortex, many critical design choices of the proposed model can be determined with some simple calculations. Comprehensive experimental evaluations demonstrate that the proposed DCNN model achieves state-of-the-art performances on four widely used benchmark datasets: CIFAR-10, CIFAR-100, SVHN and MNIST.
The integration of facial gestures and vocal signals is an essential process in social communication. Facial and vocal signals provide an abundant source of information that we use in our everyday interactions to communicate our intentions and obtain emotional and cognitive information from others. Face–voice integration relies on several brain regions, including language regions in the ventral frontal lobe. Neuroimaging has made great strides in describing activity in temporal and frontal regions during speech processing, but we have relatively little understanding of the cellular mechanisms that underlie face–voice integration in the frontal lobe. Much of the neurophysiology research into the cellular details of face and voice processing has been focused on nonhuman primates in an attempt to characterize the neural circuit involved in social communication. While much of this research has elaborated on these sensory processes in primary and secondary cortical areas, more recent research has embarked upon how higher order cortical areas like the prefrontal cortex process face and voice information. This chapter will focus on the role of the ventrolateral prefrontal cortex in the processing and integration of face and vocal information in nonhuman primates. We will first describe studies on face-responsive cells in the nonhuman primate cortex, including inferotemporal cortex and the STS and finally face processing in PFC. This will be followed by auditory responses in PFC. Finally, we will examine the integration of faces and voices by single cells in the primate prefrontal cortex and their potential role in recognition and social communication.
Psychophysical scales of a 3,3 c/deg monochromatic checkerboard of variable contrast were compared with steady state visually evoked potentials (VEP) recorded by gross electrodes on the scalp. These estimates of neuronal population responses grew as a power function of physical contrast having an exponent of approximately the same magnitude as the corresponding psychophysical function which gives credence to the validity of the procedures employed. The functional neuroimaging technique of positron emission tomography (PET), based on radioactive decay of a labelled tracer occurring inside the brain, was applied in normal subjects to quantitatively explore the influence of voluntary positive accommodation and also to examine the effect of reduced contrast sensitivity in human strabismic amblyopia. A great asymmetry in metabolic activity was observed in the striate cortex, that is, the Brodmann area 17 (BA 17) activation was strongest contralateral to the dominant viewing eye. The PET scans revealed, however, a high correlation between blood flow increases in the right striate cortex (BA 17) and the left extrastriate cortex (BA 18) during voluntary accommodation, possibly reflecting top-down modulation and reentrant processes. The poor contrast sensitivity in strabismic amblyopia could essentially be explained by deactivation of the ipsilateral extrastriate cortical areas BA 18 and BA 19.
lost her idea of ‘left,’ both with regard to the world and her own body. Sometimes (when eating) she complains that her portions are too small, but this is because she eats only from the right half of the plate—it does not occur to her that it has a left half as well. Sometimes, she will put on lipstick, and make tip the right half of her face, leaving the left half completely neglected: It is almost impossible to treat these things, because her attention cannot be drawn to them, and she has no conception that they are wrong. She knows it intellectually, and can understand, and laugh; but it is impossible for her to know it directly. (Sacks, 1985)
This chapter traces the origins of our current ideas about visual cortex. We begin, in Section 2, long before the beginning of science, in the 30th century BCE, with the earliest description of the cerebral cortex. In Section 3 we consider the views of Greek philosopher-scientists on the functions of the brain. Section 4 concerns the long period in which there were virtually no advances in Europe in understanding the brain. In Section 5 we describe how even after Western brain research was well underway again, the cerebral cortex tended to be ignored. Section 6 considers the beginning of the modern study of the cerebral cortex and the localization therein of psychological functions. Our focus narrows in Section 7 and we consider how a specifically visual area of the cortex was delineated. The final section brings us to the theme of the entire volume, the extrastriate visual cortices. This review ends in the early 1980s about the time of the award of the Nobel Prize to Hubel and Wiesel for their discoveries on the visual cortex.
The notion of a neuron that responds selectively to the image of a particular complex object has been controversial ever since Gross and his colleagues reported neurons in the temporal cortex of monkeys that were selective for the sight of a monkey's hand (Gross, Rocha-Miranda, & Bender, 1972). Since that time, evidence has mounted for neurons in the temporal lobe that respond selectively to faces. The present paper presents a critical analysis of the evidence for face neurons and discusses the implications of these neurons for models of object recognition. The paper also presents some possible reasons for the evolution of face neurons and suggests some analogies with the development of language in humans.
In primates, inferior temporal (IT) cortex is crucial for the processing and storage of visual information about form and colour. This article reviews the properties of IT neurons and considers how these properties may underlie the perceptual and mnemonic functions of IT cortex. The available evidence suggests that the processing of the facial image by IT cortex is similar to its processing of other visual patterns. Faces and other complex visual stimuli appear to be represented by the pattern of responses over a population of IT neurons rather than by the responses of specific 'feature detectors' or 'grandmother' cells. IT neurons with adult-like stimulus properties are present in monkeys as young as six weeks old.
Monkeys that were trained to perform auditory and visual short-term memory tasks (delayed matching-to-sample) received lesions
of the auditory association cortex in the superior temporal gyrus. Although visual memory was completely unaffected by the
lesions, auditory memory was severely impaired. Despite this impairment, all monkeys could discriminate sounds closer in frequency
than those used in the auditory memory task. This result suggests that the superior temporal cortex plays a role in auditory
processing and retention similar to the role the inferior temporal cortex plays in visual processing and retention.
Retinal cells have been induced to project into the medial geniculate nucleus, the principal auditory thalamic nucleus, in
newborn ferrets by reduction of targets of retinal axons in one hemisphere and creation of alternative terminal space for
these fibers in the auditory thalamus. Many cells in the medial geniculate nucleus are then visually driven, have large receptive
fields, and receive input from retinal ganglion cells with small somata and slow conduction velocities. Visual cells with
long conduction latencies and large contralateral receptive fields can also be recorded in primary auditory cortex. Some visual
cells in auditory cortex are direction selective or have oriented receptive fields that resemble those of complex cells in
primary visual cortex. Thus, functional visual projections can be routed into nonvisual structures in higher mammals, suggesting
that the modality of a sensory thalamic nucleus or cortical area may be specified by its inputs during development.
Neurons in inferotemporal cortex (area TE) of the monkey had visual receptive fields which were very large (greater than 10 by 10 degrees) and almost always included the fovea. Some extended well into both halves of the visual field, while others were confined to the ipsilateral or contralateral side. These neurons were differentially sensitive to several of the following dimensions of the stimulus: size and shape, color, orientation, and direction of movement.
Electrophysiological correlates of the processing of visual information were studied in epileptic patients with electrodes chronically implanted on the surface of striate and extrastriate cortex. In separate experiments patients viewed faces, letter strings (words and non-words), numbers, and control stimuli. A negative potential, N200, was evoked by faces, letter strings, and numbers, but not by the control stimuli. N200 was recorded bilaterally from discrete regions of the fusiform and inferior temporal gyri. These category-specific face, letter-string, and number “modules” vary in location. In most cases there was no overlap in the location of face and letter-string modules, suggesting a mosaic of functionally discrete regions. In some cases letter-string and number N200s were recorded from the same location, suggesting that these modules may be less spatially and functionally discrete. Face N200-like potentials can be recorded from temporal scalp, allowing the possibility of studying early face processing in normal subjects. Longer-latency face-specific potentials were recorded from the inferior surface of the anterior temporal lobe. Potentials evoked by colored checkerboards were recorded from a region of the fusiform gyrus posterior to the fusiform region from which category-specific N200s were recorded.
These results suggest that there are several processing streams in inferior extrastriate cortex. In addition to object recognition systems previously proposed for faces and words, our preliminary results suggest a separate system dealing with numbers. Postulated systems dealing with larger manipulable objects and animals have not been detected.
The facts recorded in this paper are partly the results of a research made conjointly by Drs. Ferrier and Yeo, aided by a grant from the British Medical Association, and partly of a research made by Dr. Ferrier alone, aided by a grant from the Royal Society. It has been considered convenient and advisable to publish the results together, more especially with the view of contrasting the different effects of lesions of different parts of the brain established under similar conditions.
The experiments which we here record were performed during the preceding winter and spring in the physiological laboratory of University College, but their formal publication has been hitherto deferred because we were desirous of keeping some of the animals in which the lesions had been established under observation during several months, in order that any modification which that lapse of time might produce in the symptoms should be duly recorded. But, although not hitherto published, several of the cases, while still under such observation, have been brought before the notice of both the Physiological and the Neurological Society of London, and have been examined at different times by various persons interested in the subject of cerebral localisation, besides being familiar to the regular workers in the laboratory. In this way we have repeatedly had the opportunity of showing most of the symptoms which we are about to record, nor have we inserted any detail as to the accuracy of which there could, to an unbiased mind, be the slightest doubt. All our experiments have been performed with the view of establishing certain lesions, uni- or bi-lateral, embracing definite areas of the cerebral cortex; and they have been confined, or nearly so, to the occipital and temporal lobes. In the performance of the operations strict antiseptic precautions were employed, the dressings being fixed by a collodion cap. On the fourth or fifth day after the operation this cap and the dressings were removed, and in every case the wound was found to be completely closed, the edges of the skin being closely united, no sign of meningitis nor of any septic mischief being at any time perceptible. In one exceptional case, however, in which the antiseptic precautions had, from over confidence, been relaxed, the asepticism was incomplete, and sloughing of the skin over the seat of operation resulted, so that the animal had to be killed within a few days of the performance of the operation. This case will be mentioned in due course.
Previous behavioral studies indicated that the inferior convexity of the temporal lobe in the rhesus monkey functions in relation to the visual system and that this function probably depends on corticocortical connections which link this area to the visual areas. Therefore, in an experimental anatomical study the corticocortical connections of some of the occipital, temporal and frontal areas were investigated in the monkey, by means of the Nauta-Gygax silver impregnation technique. The following findings were obtained. The striate cortex projects to certain parts of a “circumstriate cortical belt” which extends into the caudal bank of the superior temporal sulcus in its upper parts and into the caudal parts of the intraparietal sulcus. This circumstriate belt in turn projects to the inferior convexity of the temporal lobe and to the cortex around the arcuate sulcus of the frontal lobe. The inferior convexity of the temporal lobe in turn projects back to parts of the circumstriate belt and to the lateral and the ventrolateral surface of the frontal lobe.
ocular and head movements upon cortical stimulation (pupil dilation) in dog, monkey; describes electric stimulation of temporal lobe of monkey; pricking up of ears and moving eyes as toward imagined sound, with pupillary dilation no Ferrier, D. (1889). 'Schaefer on the temporal and occipital lobes.' Brain: A Journal of Neurology, v11:7-30.
The activity of neurons in inferior temporal cortex of behaving monkeys was studied under the following conditions: (1) in untrained animals as they spontaneously fixated visual stimuli, (2) in an animal with immobilization of one eye after section of the oculomotor nerves, (3) during performance of a visual discrimination task and (4) during performance of a visual recent memory task. When stimulated through the immobilized eye, the properties of inferior temporal were similar to those seen under anesthesia and total immobilization. Under the other conditions, the response properties of inferior temporal neurons appeared to be modulated by attentional and situational variables.
Visual receptive fields and responsiveness of neurons to somesthetic and auditory stimuli were studied in the inferior temporal cortex and adjacent regions of immobilized macaques. Neurons throughout cytoarchitectonic area TE were responsive only to visual stimuli and had large receptive fields that almost always included the center of gaze and usually extended into both visual half-fields. There was no indication of any visuotopic organization within area TE. Neurons in an anterior and in a dorsal portion of TE tended to have larger receptive fields. By contrast, dorsal, ventral and anterior to area TE, units often responded to somesthetic and auditory as well as to visual stimuli. In these regions visual receptive fields were even larger than in TE and often included the entire visual field. Posterior to TE the neurons were exclusively visual and had much smaller receptive fields that were confined to the contralateral visual field and were topographically organized.
Separate groups of monkeys were trained on delayed object alternation, delayed object matching, and delayed color matching, after which half the animals in each group received lesions of the cortex in the principal sulcus, and the other half, lesions of the inferior frontal convexity. The inferior convexity lesions produced severe and lasting impairments on all three tasks, perhaps as a result of the perseverative disorder that has been associated with damage to this region. By contrast, the principal sulcus lesions, which yield such severe deficits on spatial memory tasks, led to only small, transient disruptions on each of the three non-spatial tasks. According to these results, the non-spatial memory deficits that have been found after unrestricted lateral prefrontal lesions are due mainly to damage below the principal sulcus in the inferior prefrontal cortex. The function of the tissue in the principal sulcus itself, on the other hand, appears so far to be limited largely to the spatial modality.
Accumulating neuropsychological, electrophysiological and behavioural evidence suggests that the neural substrates of visual perception may be quite distinct from those underlying the visual control of actions. In other words, the set of object descriptions that permit identification and recognition may be computed independently of the set of descriptions that allow an observer to shape the hand appropriately to pick up an object. We propose that the ventral stream of projections from the striate cortex to the inferotemporal cortex plays the major role in the perceptual identification of objects, while the dorsal stream projecting from the striate cortex to the posterior parietal region mediates the required sensorimotor transformations for visually guided actions directed at such objects.
The inferior temporal gyrus in the monkey appears to be unique among the many extrastriate visual cortices in its importance for normal performance of delayed match-to-sample, a visual memory task. However, the anatomical pathway providing visual information to this portion of the temporal lobe remains unclear. In this study, wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) was injected into the anterior inferior temporal gyrus and heavy projections were found to arise in cytoarchitectural area TF of the parahippocampal gyrus, as well as moderate projections in more posterior portions of inferior temporal gyrus and perirhinal and entorhinal cortices. Subsequently, WGA-HRP was injected into area TF, resulting in retrogradely labeled cells primarily located in the portions of area TF adjacent to the injection and also in the occipitotemporal sulcus including the ventral portion of the prestriate visual area V4. Moderate projections were found to originate from the dorsal region of area V4 in the lunate sulcus, portions of the caudal parietal lobe, the posterior bank of caudal superior temporal sulcus, and area OPT located at the tip of the superior temporal sulcus. The middle temporal gyrus, foveal prestriate cortex, and area TEO, a transitional area between temporal and occipital visual areas, were all free from retrogradely labeled cells. These latter areas are included in the well-established anatomical system that is known to carry visual information from striate cortex through prestriate to eventually reach dorsal portions of inferotemporal cortex which is coincident with the temporal lobe visual area TE. It is suggested here that there is an additional ventral pathway into area TE as well, which includes projections through portions of the prestriate cortex, occipitotemporal sulcus, and parahippocampal gyrus, ultimately reaching the anterior inferior temporal gyrus, an area that may be specialized to hold visual information over brief periods of time.
The inferotemporal cortex of primates plays a prominent role in the learning and retention of visual form discriminations. In this experiment we investigated the role of inferotemporal (IT) cortex in the discrimination of two-dimensional forms defined by motion cues. Six monkeys were trained to a criterion level of performance on two form-from-motion problems. Three of these animals received complete bilateral lesions of IT cortex, while the other three served as unoperated controls. All animals were then retrained to criterion to evaluate the effects of IT lesions on the retention of form-from-motion learning. Compared with the control group, the lesion group was significantly impaired on both problems. Following retention testing, we trained both groups of monkeys on two new form-from-motion problems to investigate the effects of IT lesions on acquisition rates for new learning. The lesion group performed well on the new problems; the learning rates of the operated and control groups were not significantly different. When forms were defined by luminance cues, monkeys with IT lesions, like those in previous studies, were impaired both for retention and for acquisition. These findings indicate that the anterograde effects of IT lesions on learning new form discriminations are less severe for forms defined by motion cues than for forms defined by luminance cues. However, the retrograde effects of IT lesions on retention are severe for forms defined by either cue.
The sources of ipsilateral cortical afferent projections to basoventral and mediodorsal prefrontal cortices that receive some visual input were studied with retrograde tracers (horseradish peroxidase or fluorescent dyes) in eight rhesus monkeys. The basoventral regions injected with tracers included basal (orbital) areas 11 and 12, lateral area 12, and ventral area 46. The mediodorsal regions included portions of medial area 32 and the caudal part of dorsal area 8. These sites represent areas within basoventral and mediodorsal prefrontal cortices that show a gradual increase in architectonic differentiation in a direction from the least differentiated orbital and medial limbic cortices toward the most differentiated cortices in the arcuate concavity. The results showed that the visual input to basoventral and mediodorsal prefrontal cortices originated largely in topographically distinct visual areas. Thus, basoventral sites received most of their visual cortical projections from the inferior temporal cortex. The rostral inferior temporal region was the predominant source of visual projections to orbital prefrontal sites, whereas lateral area 12 and ventral area 46 also received projections which were found more caudally. In contrast, mediodorsal prefrontal sites received most of their visual projections from dorsolateral and dorsomedial visual areas. The cells of origin were located in rostromedial visual cortices after injection of retrograde tracers in area 32 and in more caudal medial and dorsolateral visual areas after injection in caudal area 8. The latter also received substantial projections from visuomotor regions in the caudal portion of the lateral bank of the intraparietal sulcus. These results suggest that the basoventral prefrontal cortices are connected with ventral visual areas implicated in pattern recognition and discrimination, whereas the mediodorsal cortices are connected with medial and dorsolateral occipital and parietal areas associated with visuospatial functions. In addition, the prefrontal areas studied received projections from auditory and/or somatosensory cortices, from areas associated with more than one modality, and from limbic regions. Orbital area 12 seemed to be a major target of projections from somatosensory cortices and the rostral portion of medial area 32 received substantial projections from auditory cortices. The least architectonically differentiated areas (orbital area 11 and medial area 32) had more widespread corticocortical connections, including strong links with limbic cortices.(ABSTRACT TRUNCATED AT 400 WORDS)
Anatomical and physiological observations in monkeys indicate that the primate visual system consists of several separate and independent subdivisions that analyze different aspects of the same retinal image: cells in cortical visual areas 1 and 2 and higher visual areas are segregated into three interdigitating subdivisions that differ in their selectivity for color, stereopsis, movement, and orientation. The pathways selective for form and color seem to be derived mainly from the parvocellular geniculate subdivisions, the depth- and movement-selective components from the magnocellular. At lower levels, in the retina and in the geniculate, cells in these two subdivisions differ in their color selectivity, contrast sensitivity, temporal properties, and spatial resolution. These major differences in the properties of cells at lower levels in each of the subdivisions led to the prediction that different visual functions, such as color, depth, movement, and form perception, should exhibit corresponding differences. Human perceptual experiments are remarkably consistent with these predictions. Moreover, perceptual experiments can be designed to ask which subdivisions of the system are responsible for particular visual abilities, such as figure/ground discrimination or perception of depth from perspective or relative movement--functions that might be difficult to deduce from single-cell response properties.
Visual receptive fields of single neurons and clusters of neurons were determined for recording sites in the occipital, caudal temporal and caudal parietal lobes of the owl monkey. In 7 experiments the visuotopic organization of the caudal third of the middle temporal gyrus was explored and a complete representation of the contralateral half of the visual field was revealed. This representation of the visual field (MT) corresponds to a histologically distinct area adjacent and rostral to area 19. The MT area is oval with its major axis approximately 6 mm long rostrocaudally and 4–5 mm wide mediolaterally. The horizontal meridian divides MT into a lateral portion representing the upper visual quadrant and a medial portion representing the lower quadrant. The center of gaze is reprented in the caudal portion of MT bordering area 19. The representation of the periphery of the visual field lies in rostral MT immediately medial and caudal to the caudal tip of the superior temporal sulcus.
The [2-14C]deoxyglucose method was used to identify the cerebral areas related to vision in the rhesus monkey (Macaca mulatta). This was achieved by comparing glucose utilization in a visually stimulated with that in a visually deafferented hemisphere. The cortical areas related to vision included the entire expanse of striate, prestriate, and inferior temporal cortex as far forward as the temporal pole, the posterior part of the inferior parietal lobule, and the prearcuate and inferior prefrontal cortex. Subcortically, in addition to the dorsal lateral geniculate nucleus and superficial layers of the superior colliculus, and structures related to vision included large parts of the pulvinar, caudate, putamen, claustrum, and amygdala. These results, which are consonant with a model of visual function that postulates an occipito-temporo-prefrontal pathway for object vision and an occipito-parieto-prefrontal pathway for spatial vision, reveal the full extent of those pathways and identify their points of contact with limbic, striatal, and diencephalic structures.
The representation of the visual field in the area adjacent to striate cortex was mapped with multiunit electrodes in the macaque. The animals were immobilized and anesthetized and in each animal 30 to 40 electrode penetrations were typically made over several recording sessions.
This area, V2, contains a topographically organized representation of the contralateral visual field up to an eccentricity of at least 80°. The representation of the vertical meridian is adjacent to that in striate cortex (V1) and forms the posterior border of V2. The representation of the horizontal meridian in V2 forms the anterior border of V2 and is split so that the representation of the lower visual field is located dorsally and that of the upper field ventrally. As in V1, the representation of the central visual field is magnified relative to that of the periphery. The area of V2 is slightly smaller than that of V1. At a given eccentricity, receptive field size in V2 is larger than in V1.
The myeloarchitecture of V2 is distinguishable from that of the surrounding cortex. The location of V2 corresponds, at least approximately, to that of cytoarchitectonic Area OB. V2 is bordered anteriorly by several other areas containing representations of the visual field.
Inferior temporal cortex is perhaps the highest visual processing area and much anatomical work has focused on its connections with other visual areas in temporal and occipital cortex. Here we report connections of inferior temporal cortex with regions in the frontal and parietal lobes. Inferior temporal areas TEO and TE were injected with WGA-HRP and 3H-AA, respectively, or vice versa, in 1-week-old infant and 3-4-year-old adult monkeys (Macaca mulatta). The results indicated that whereas TEO has more extensive connections with parietal areas, TE has more extensive connections with prefrontal areas. Thus, in the intraparietal sulcus, area TEO is connected with areas LIPd, LIPv, and V3A, and with the as yet undefined region between LIPv and V3A, whereas the connections of TE are predominantly with LIPd, and to a lesser extent with LIPv. In the prefrontal cortex, area TE is connected with areas 8 and 45 in the inferior limb of the anterior bank of the arcuate sulcus, with area 12 on the inferior prefrontal convexity, and with areas 11 and 13 on the orbital surface. By contrast, the connections of area TEO are limited to areas 8, 45, and 12. Furthermore, within prefrontal cortex, the projections from areas TEO and TE terminate in different layers in areas 8 and 45, such that those from TEO terminate in all layers, whereas those from TEO terminate in layers I and V/VI only. In contrast to the connections of areas TEO and TE with various medial temporal-lobe and subcortical structures, which are immature in infant monkeys (Webster et al., 1991, 1993b), the connections with parietal and prefrontal areas appear adult-like as early as 1 week of age.
Anatomical and physiological investigations indicate two major distinct functional streams within the extrastriate visual cortex of the macaque monkey, and behavioral observations suggest that the ventral (occipitotemporal) pathway is the cornerstone for object recognition whereas the dorsal (occipitoparietal) pathway is primarily involved in visuospatial perception and visuomotor performance. In the context of this dichotomy we conducted a psychophysical and neuropsychological study of visual perceptual abilities in two stroke patients, each with lesions involving several extrastriate areas. Magnetic resonance imaging demonstrated bilateral lesions; in one patient (E.W.) the lesion involves the ventral medial portions of the occipital and temporal lobes, and in the other (A.F.) the lesion involves dorsally the occipital-parietal area, including the region of the temporal-parietal-occipital junction. E.W. suffers from achromatopsia of central origin, prosopagnosia, visual agnosia, and alexia without agraphia. His depth and motion perception, including recognition of moving objects, are normal. He has superior visual field loss bilaterally, and slightly impaired acuity, and complains that the world appears in a deep twilight even on a sunny day. In contrast, A.F. shows specific deficits of stereopsis, spatial localization, and several aspects of motion perception. He is also impaired at recognizing objects presented from unconventional views, but recognition of prototypical views of objects, and color and form discrimination are normal, as is his ability to recognize faces. The anatomical characteristics of the lesions of these two patients permit a direct experimental comparison of the effects of lesions confined to the parietal or temporal pathways. E.W.'s and A.F.'s performance on the psychophysical and neuropsychological tasks discussed here supports the functional distinction between a dorsal and a ventral extrastriate system but additionally suggests the existence of a pathway involved in identification-from-motion that is separate from both the dorsal early motion/spatial analysis pathway and the ventral color/static-form pathway.
The physiological properties of neurons in inferior temporal (IT) cortex of the macaque monkey suggest that this cortical area plays a major role in visual pattern recognition. Based on the properties of IT, and one of its major sources of input, V4, a model is proposed that can account for some of the shape recognition properties of IT neurons including selectivity for complex visual stimuli and tolerance to the size and location of the stimuli. The model is composed of three components. First, stimulus location tolerance is modeled after the complex-cell-like properties observed in some V4 neurons. The second component of the model is an attentionally controlled scaling mechanism that facilitates size-invariant shape recognition. The transition from edge orientation-selective neurons in V4 to neurons with more complicated stimulus preference in IT is explained by the third component of the model, a competitive learning mechanism. Single-unit analysis of receptive field properties, stimulus selectivity, and stimulus size and position tolerance was performed on "neurons" from the simulation. Comparison of results from the simulation and a study of actual IT neurons shows that the set of mechanisms incorporated into the simulation is sufficient to emulate the physiological data.
The specific size and retinal location of an object are readily perceived, yet recognition of an object's identity is hardly affected by transformations of its size or location. To explore how such stimulus transformations are treated by known mechanisms for visual short-term memory in inferior temporal (IT) cortex, IT cells were recorded in monkeys performing a delayed matching-to-sample task. The stimuli were pictures of complex objects, and the monkeys ignored differences in size and retinal location when matching the test items to the sample held in memory. The sensory information communicated by cells was assessed in their responses to the sample stimuli, and mnemonic information was assessed in their responses to the test stimuli. In the sensory domain, the ordering of relative stimulus preferences for nearly all cells was invariant over changes in size or location; however, some cells nonetheless preferred stimuli of a given size or location. In the mnemonic domain, the responses of many cells were modulated according to whether the test stimulus matched the sample held in memory, and these memory effects were invariant over the relative sizes and locations of the stimuli. Thus, IT neuronal populations may mediate not only the recognition and memory of object identity, which are invariant over size and location, but also the perception of the transformations themselves.
We investigated the role that different component parts play in the neural encoding of the visual appearance of one complex object in the temporal cortex. Cells responsive to the sight of the entire human body (but no to control stimuli) were tested with two subregions (head alone with the body occluded from sight and the body alone with the head occluded). Forty-two percent (22 of 53) of cells responded to the whole body and to one of the two body regions tested separately: 72% (17 of 22) responding to the head and 28% (5 of 22) to the rest of the body. Forty-two percent (22 of 53) of cells responded independently to both regions of the body when tested in isolation. The remaining cells (17%, 9 of 53) were selective for the entire body and unresponsive to component parts. The majority of cells tested (90%, 35 of 39) were selective for perspective view (e.g., some cells respond optimally to the side view of the body, others to the back view). Comparable levels of view sensitivity were found for responses to the whole body and its parts. Results indicate (1) separate neuronal analysis of body parts and (2) extensive integration of information from different parts. Contrary to influential models of object recognition (Marr and Nishihara, 1978; Biederman, 1987), the results indicate view-specific processing both for the appearance of separate object components and for integration of information across components.
Inferior temporal (IT) cortex is critical for visual pattern recognition in adult primates. However, the functional development of IT cortex appears to be incomplete until late in the first year of life in monkeys and probably beyond. Responses of neurons in IT are substantially weaker, of longer latency, and more susceptible to anesthesia within at least the first half year of life. In addition, refinement of connections of IT, particularly those with regions in the opposite hemisphere and with regions related to memory and attention, continues for at least several months after birth. Moreover, many of the pattern recognition functions that IT supports in adulthood themselves show a very protracted period of development, and damage to IT cortex in infancy appears to have relatively little effect on pattern recognition abilities, despite the pronounced effects of comparable damage in adulthood. These findings all suggest that IT undergoes an extended period of postnatal development, during which both visual experience and the maturation of other brain structures may contribute to the emergence of mechanisms of pattern recognition within IT. In other respects, fundamental characteristics of IT emerge quite early. For example, despite their weaker responses, IT neurons have adult-like patterns of responsiveness--including pronounced form selectivity and large bilateral receptive fields--as early as we were able to test (approximately 6 weeks). Thus, IT cortex appears to be prewired with (or predisposed to develop rapidly) neural circuitry sufficient to produce basic properties remarkably similar to those found in the adult animal. Future studies of IT cortex will need to address the development of signals related to perceptual constancies and to formation and retrieval of visual object memories, the development of interactions with other regions involved in visual recognition (particularly frontal cortex), and the specific mechanisms underlying various types of plasticity present in IT cortex in both developing and mature primates.
Areas and pathways subserving object and spatial vision are segregated in the visual system. Experiments show that the primate prefrontal cortex is similarly segregated into object and spatial domains. Neurons that code information related to stimulus identity are dissociable, both by function and region, from those that code information related to stimulus location. These findings indicate that the prefrontal cortex contains separate processing mechanisms for remembering "what" and "where" an object is.
The effects of temporal lobectomy, lateral surface or ventral surface-hippocampal ablations on acquisition and retention of visual discriminations in the baboon are reported. Total lobectomy and ventral-hippocampal ablation produced deficits more marked in original learning than in retention. Lateral resection had little effect on visual discrimination, and in none of the animals was there impairment of delayed responses.
After preliminary training on visual discriminations and on other visual function tests, three macaques received bilateral ablations of the ventral temporal cortex, bilateral removal of the hippocampal formation in three others, and two received control operations reproducing the cortical damage incidental to the experimental operations. The greatest decrement in visual discrimination occurred in the temporal lobe group, the amount of retardation being a function of the difficulty of the discriminations. Impairment of visual discrimination was not correlated with performance in the other tasks.
In this paper, we analyze the activity of single fibers in the optic nerve of a frog. Our method is to find what sort of stimulus causes the largest activity in one nerve fiber and then what is the exciting aspect of that stimulus such that variations in everything else cause little change in the response. It has been known for the past 20 years that each fiber is connected not to a few rods and cones in the retina but to very many over a fair area. Our results show that for the most part within that area, it is not the light intensity itself but rather the pattern of local variation of intensity that is the exciting factor. There are four types of fibers, each type concerned with a different sort of pattern. Each type is uniformly distributed over the whole retina of the frog. Thus, there are four distinct parallel distributed channels whereby the frog's eye informs his brain about the visual image in terms of local pattern independent of average illumination. We describe the patterns and show the functional and anatomical separation of the channels. This work has been done on the frog, and our interpretation applies only to the frog.