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Location of injection sites. Upper part: composite view of all the injection sites mapped on a template right hemisphere. Each injection site was numbered and reported, based on anatomical landmarks and stereotaxic coordinates, in the posterior bank of the arcuate sulcus ( A ) in the IPL ( B ), and in the VLPF ( C ). In order to avoid distortions of the template hemisphere, the AP level of the injections sites in anterior intraparietal (AIP) in the ventral bank of the inferior parietal sulcus and in rostral area 46vc in the ventral bank of PS is indicated by arrows. Arrowheads in B indicate the rostro-caudal extent of area AIP , which does not extend on the lateral surface. Lower part: the location of injection sites in Cases 30l WGA-HRP ( D ), 54r FR and BDA ( E ), and 55r FR and 43r LYD ( F ), shown on dorsolateral views of the injected hemispheres and in coronal sections through the core (shown in black) and the halo (shown in lighter gray). The arrows in the dorsolateral views of the hemispheres in D , E , and F indicate the levels of the injection sites within sulci. For the sake of comparison, all the reconstructions in this fi gure are shown as a right hemisphere. Cg, cingulate sulcus; LO, lateral orbital sulcus; Lu, lunate sulcus; MO, medial orbital sulcus. Other abbreviations as in Figure 1.
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We found that the macaque inferior parietal (PFG and anterior intraparietal [AIP]), ventral premotor (F5p and F5a), and ventrolateral prefrontal (rostral 46vc and intermediate 12r) areas forming a network involved in controlling purposeful hand actions ("lateral grasping network") are a source of corticotectal projections. Based on injections of an...
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Context 1
... injection sites used in the present study involved PMv, IPL, and VLPF areas or fi elds, which, based on their cortical connectivity, appear to form a network involved in selecting and controlling goal-directed hand actions, here designated as the lateral grasping network. Figure 3 shows in the upper part a composite view of the location of all the injection sites and in the lower part the exact location of those injection sites not previously published. In the PMv, 2 tracer injections (Cases 34l BDA and 30l WGA-HRP) were placed in F5a, a visuomotor hand-related fi eld (Theys et al. 2012) tightly connected to F5p and displaying consistent connections with the IPL areas AIP and PFG and with the prefrontal areas 46v and 12r (Gerbella et al. 2011). In the IPL, 2 tracer injections (Cases 14r BDA and 54r FR) involved PFG, a visuomotor hand-related area (Rozzi et al. 2008) consistently connected both to F5p and F5a and to area 46v (Rozzi et al. 2006). Two other tracer injections (Cases 30l BDA and 54r BDA) involved AIP, a visuomotor hand-related area (Murata et al. 2000) consistently connected both to F5p and F5a and to the prefrontal areas 46v and 12r (Borra et al. 2008). In the VLPF, 2 tracer injections (Cases 43r LYD and 52r BDA) were placed in the caudal part of area 46v (46vc), at about 5 – 6 mm from the caudal border. These injections involved a sector of this area (rostral 46vc), displaying consistent connections with F5a, PFG, and AIP (Gerbella et al. 2012). Three other VLPF tracer injections (Cases 44r LYD and FR, and 55r FR) involved the intermediate part of area 12r (intermediate 12r), that is, the sector consistently connected to F5a and AIP (Borra et al. 2011). Finally, the previously published data from one representative case (Case 35r BDA) of tracer injection in area F5p were reanalyzed here to allow a comparison of the corticotectal projections of this area with those of the other areas of the hand action cortical network. The results showed that all the areas of the lateral grasping network are a source of projections to the mesencephalon, mostly involving the SC and the adjacent mesencephalic reticular formation (MRF). Additional dense spots of labeled terminals were observed in the pontine nuclei after tracer injections in areas F5a, PFG, and AIP. Furthermore, after tracer injections in area F5a, some anterograde labeling was observed in the pontine reticular formation. Thus, the brainstem projections of F5a were similar to those of F5p, which, however, also projects to the bulbar reticular formation (Borra et al. 2010). The distribution of anterograde labeling observed in the mesencephalon after injections in the various areas of the lateral grasping network is shown in Figures 4 – 7 in drawings of selected coronal sections through the brainstem and in 2D reconstructions of the ipsilateral SC. In spite of some variability observed across the cases, all the injected areas displayed several common connectional features in their projections to the mesencephalic structures. First, relatively dense anterograde labeling was observed in the ipsilateral SC, in the intermediate and the deep gray layers (stratum griseum intermediale [SGI] and stratum griseum profundum [SGP], respectively), but not in the super fi cial layers. Secondly, the labeling in the ipsilateral SC tended to be richer in the lateral part along almost the entire rostro-caudal extent. Thirdly, though with some variability, anterograde labeling extended from the lateral part of the SGP to the ventrally adjacent MRF. All these connectional features also character- ized the corticotectal projections from F5p. Besides these common connectional features, some differences were observed across the cases, mostly in the distribution of anterograde labeling in the ipsilateral SC. Speci fi cally, after tracer injections in the IPL and VLPF areas, in most of the cases, the labeling tended to be more extensive and was relatively rich also more medially. Furthermore, some labeled terminals were observed in the SGI of the contralateral SC (not shown) in all cases, but those of VLPF tracer injections. This contralateral labeling showed a distribution similar to that observed in the ipsilateral SC, but was consider- ably less rich and extensive. Finally, in those cases in which the labeling in the MRF appeared to be more extensive (e.g., Cases 30l WGA-HRP and 52r BDA, Figs 4 and 6), some anterograde labeling was also observed in the periaqueductal gray. The relatively limited number of tracer injections on which the present study is based does not allow us to draw any fi rm conclusion about whether these differences are due to true interareal connectional differences or due to some unavoidable variability intrinsic to the tract-tracing experimental approach used in the present study. In all cases, anterograde labeling in the SC, particularly in the lateral part, tended to be organized into 2 distinct zones, located in the SGI and SGP, respectively (Fig. 8 A , D , E ). Speci fi cally, preterminal arborizations, varicosities, and synaptic endings tended to be relatively more packed in the SGI and more loosely arranged in the SGP as well as in the adjacent MRF (Fig. 8 B , C ). Furthermore, labeled axons within and in ...
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Saccadic eye movements play a central role in primate vision. Yet, relatively little is known about their effects on the neural processing of visual inputs. Here we examine this question in primary visual cortex (V1) using receptive-field-based models, combined with an experimental design that leaves the retinal stimulus unaffected by saccades. Thi...
Citations
... In a control condition of this experiment, the subjects responded to visual oddball stimuli with a single button press but, in contrast to the paradigm reported by Nagy et al. 10 , without reaching movements (please refer to Prabhu and Himmelbach 9 for more details). Anatomical studies in macaques reported connections between the upper limb motor region of the SC and the ventral premotor cortex (PMv [11][12][13] ) and dorsal premotor cortex (PMd 11,13,14 ). The involvement of the ventral and dorsal premotor cortex in the execution of simple and complex finger tapping movements has been shown repeatedly in human fMRI studies [15][16][17][18][19] (please refer to Witt et al. 20 for a meta-analysis of 38 studies). ...
... The premotor cortices, PMd and PMv, have been implicated in the integration of sensory information towards the realization of sequential movements [15][16][17][18][19] (please see Witt et al. 20 for a meta-analysis). Studies by Fries 11 , Borra et al. 12 , Distler and Hoffmann 14 , and Fregosi and Rouiller 13 described connections between the ventral and dorsal premotor cortices and the SC limb motor region. Results of our earlier study on tactile reaching movements included a control condition with button presses that showed a response in the SC motor region 9 . ...
Electrophysiological studies in macaques and functional neuroimaging in humans revealed a motor region in the superior colliculus (SC) for upper limb reaching movements. Connectivity studies in macaques reported direct connections between this SC motor region and cortical premotor arm, hand, and finger regions. These findings motivated us to investigate if the human SC is also involved in sequential finger tapping movements. We analyzed fMRI task data of 130 subjects executing finger tapping from the Human Connectome Project. While we found strong signals in the SC for visual cues, we found no signals related to simple finger tapping. In subsequent experimental measurements, we searched for responses in the SC corresponding to complex above simple finger tapping sequences. We observed expected signal increases in cortical motor and premotor regions for complex compared to simple finger tapping, but no signal increases in the motor region of the SC. Despite evidence for direct anatomical connections of the SC motor region and cortical premotor hand and finger areas in macaques, our results suggest that the SC is not involved in simple or complex finger tapping in humans.
... Early retrograde tracing studies by Fries et al. (1985) found projections to the SC from all of the abovementioned cortical areas in macaques. Borra et al. (2014) later reported projections to the SC from PMv with higher precision, while Distler and Hoffman (2015) found connections from PMd to the SC. This anatomical SC connectivity supported reports of the functional involvement of the SC in reaching in macaques and humans (Werner ...
The superior colliculus (SC) plays a major role in orienting movements of eyes and the head and in the allocation of attention. Functions of the SC have been mostly investigated in animal models, including non-human primates. Differences in the SC's anatomy and function between different species question extrapolations of these studies to humans without further validation. Few electrophysiological and neuroimaging studies in animal models and humans have reported a role of the SC in visually guided reaching movements. Using BOLD fMRI imaging, we sought to decipher if the SC is also active during reaching movements guided by tactile stimulation. Participants executed reaching movements to visual and tactile target positions. When contrasted against visual and tactile stimulation without reaching, we found increased SC activity with reaching not only for visual but also for tactile targets. We conclude that the SC's involvement in reaching does not rely on visual inputs. It is also independent from a specific sensory modality. Our results indicate a general involvement of the human SC in upper limb reaching movements.
... The arc in the graph indicates the direction of causal relationship, and the number above represents the weight for the edge. direct connections with the motor systems that control the head and eye movements, eye muscles, and the limbs (Baizer and Desimone 1993;Borra et al. 2014;Glickstein et al. 1985;Qian et al. 2016). Furthermore, its interconnections with the ventral stream also play an important role in regulating complex and f lexible visuomotor skills (Milner 2017). ...
The mental flow that commonly emerges during immersion in artistic activities is beneficial for maintaining mental health. However, there is not that much converging neurobiological evidence about how flow emerges and elicits pleasure in arts. Using an imitation task of Chinese calligraphic handwriting with self-rated subjective flow experience, we investigated the neural interactions supporting flow. Our results show that calligraphic handwriting requires cooperation between widespread multimodal regions that span the visual and sensorimotor areas along the dorsal stream, the top-down attentional control system, and the orbito-affective network. We demonstrate that higher flow is characterized by an efficiently working brain that manifests as less activation particularly in the brain regions within dorsal attention network and functional connectivity between visual and sensorimotor networks in calligraphy. Furthermore, we also propose that pleasure during calligraphy writing arises from efficient cortical activity in the emergence of flow, and the orbito-caudate circuit responsible for feelings of affection. These findings provide new insight into the neuropsychological representations of flow through art, and highlight the potential benefits of artistic activities to boost well-being and prosperity.
... The MNS underlie imitative functions (for reviews and meta-analysis see Caspers et al. 2010;Molenberghs et al. 2012;Van Overwalle and Baetens 2009), and lesions to the MNS core regions affected -critically and to a similar extent -not only the imitation, but also the recognition of actions and gestures (Binder et al. 2017). Crucially, during the imitation of novel sequential actions, the MNS works in conjunction with other neural structures, such as the dorso-lateral prefrontal cortex (Sakreida et al. 2018) and superior temporal cortex (Oh et al. 2019), which are anatomically connected with the MNS (Borra et al. 2014(Borra et al. , 2017 and underlie mindreading functions. ...
In this paper, we propose the expression cognitive twists for cognitive mechanisms that result from the coevolution of genes and learning. Evidence is available that at least some cultural learning mechanisms, such as imitation and language, have evolved genetically under the pressure produced by culture, even though they are mostly acquired through domain-general learning during development. Although the existence of these mechanisms is consistent with evolutionary theory, their importance has not been sufficiently emphasized by mind-centered accounts of human cognitive evolution, namely evolutionary psychology and cultural evolutionary psychology. We provide concrete examples of cognitive twists, such as vocal imitation. Genetic changes in action-perception matching circuits suggest that human imitation and perhaps language are cognitive twists, namely plastic, learnable, yet genetically evolved cognitive mechanisms. We conclude that cognitive twists depict plausible evolutionary scenarios for the evolution of cognition in Homo sapiens.
... One such action circuitry is the loop between prefrontal cortex and basal ganglia which is involved in gaze control 8,9 . Prefrontal cortex is known to be sensitive to object novelty 10,11 even from childhood 12 . ...
... Together these results suggest vlPFC to encode a common currency signal related the attention worthiness of objects. This is consistent with the role of vlPFC in controlling gaze via anatomical projections to frontal eye field (FEF) 29 and superior colliculus (SC) 9 . cdlSNr showed significant coding of salient aversive objects similar to appetitive objects. ...
... These results along with previous electrophysiological and anatomical findings 9,19,24,27,29,[39][40][41][42][43][44][45] , help reveal the outlines of the circuit model involved in object salience memory (Fig. 7). Based on this model, vlPFC receives novelty and recency information from IT cortex 46 and value/aversiveness information from basal ganglia output, cdlSNr, via the medial nucleus of thalamus 43 consistent with its role as an information hub for mediating behavior in multifaceted and complex contexts [47][48][49][50] . ...
Ecological fitness depends on maintaining object histories to guide future interactions. Recent evidence shows that value memory changes passive visual responses to objects in ventrolateral prefrontal cortex (vlPFC) and substantia nigra reticulata (SNr). However, it is not known whether this effect is limited to reward history and if not how cross-domain representations are organized within the same or different neural populations in this corticobasal circuitry. To address this issue, visual responses of the same neurons across appetitive, aversive and novelty domains were recorded in vlPFC and SNr. Results showed that changes in visual responses across domains happened in the same rather than separate populations and were related to salience rather than valence of objects. Furthermore, while SNr preferentially encoded outcome related salience memory, vlPFC encoded salience memory across all domains in a correlated fashion, consistent with its role as an information hub to guide behavior.
... The SCi regulates saccadic eye movement, whereas the SCd receives dense projections from the primary and supplementary motor cortices [102]. The SCi and the SCd function as a midbrain sensorimotor structure and receive a moderate projection from the dorsal and ventral premotor cortex, the anterior and lateral intraparietal cortex, the inferior parietal cortex (inferior parietal lobule area 7b), and the ventrolateral prefrontal areas [103][104][105], forming a network involved in the control of purposeful hand actions. In rhesus monkeys, cells in rostrolateral regions of the SNr project largely to lateral portions of the SC [106]. ...
The superior colliculus (SC), one of the most well-characterized midbrain sensorimotor structures where visual, auditory, and somatosensory information are integrated to initiate motor commands, is highly conserved across vertebrate evolution. Moreover, cell-type-specific SC neurons integrate afferent signals within local networks to generate defined output related to innate and cognitive behaviors. This review focuses on the recent progress in understanding of phenotypic diversity amongst SC neurons and their intrinsic circuits and long-projection targets. We further describe relevant neural circuits and specific cell types in relation to behavioral outputs and cognitive functions. The systematic delineation of SC organization, cell types, and neural connections is further put into context across species as these depend upon laminar architecture. Moreover, we focus on SC neural circuitry involving saccadic eye movement, and cognitive and innate behaviors. Overall, the review provides insight into SC functioning and represents a basis for further understanding of the pathology associated with SC dysfunction.
... However, it is still unknown whether they send any feedback projections to these sensory cortices (Figure 2b, j). Research has shown that the SC receives anatomical projections from the PFC and the PPC (Borra, Gerbella, Rozzi, Tonelli, & Luppino, 2014;Johnston & Everling, 2006), the latter one having cortico-cortical or anatomical connections with the visual cortex, auditory cortex, and the PFC (Hovde et al., 2018;Olsen et al., 2019;Whitlock, 2017). On the other hand, the IC that lies caudal to the SC has projections not only from the auditory cortex but from non-auditory areas as well, such as somatosensory cortex, visual cortex, and motor cortex (Lesicko et al., 2016;Olthof, Rees, & Gartside, 2019;Yang et al., 2020). ...
Objective:
Neuroplasticity enables the brain to establish new crossmodal connections or reorganize old connections which are essential to perceiving a multisensorial world. The intent of this review is to identify and summarize the current developments in neuroplasticity and crossmodal connectivity, and deepen understanding of how crossmodal connectivity develops in the normal, healthy brain, highlighting novel perspectives about the principles that guide this connectivity.
Methods:
To the above end, a narrative review is carried out. The data documented in prior relevant studies in neuroscience, psychology and other related fields available in a wide range of prominent electronic databases are critically assessed, synthesized, interpreted with qualitative rather than quantitative elements, and linked together to form new propositions and hypotheses about neuroplasticity and crossmodal connectivity.
Results:
Three major themes are identified. First, it appears that neuroplasticity operates by following eight fundamental principles and crossmodal integration operates by following three principles. Second, two different forms of crossmodal connectivity, namely direct crossmodal connectivity and indirect crossmodal connectivity, are suggested to operate in both unisensory and multisensory perception. Third, three principles possibly guide the development of crossmodal connectivity into adulthood. These are labeled as the principle of innate crossmodality, the principle of evolution-driven 'neuromodular' reorganization and the principle of multimodal experience. These principles are combined to develop a three-factor interaction model of crossmodal connectivity.
Conclusions:
The hypothesized principles and the proposed model together advance understanding of neuroplasticity, the nature of crossmodal connectivity, and how such connectivity develops in the normal, healthy brain.
... We focused on the midbrain superior colliculus (SC), a key brain region in sensorimotor decisions. SC receives input from diverse sensory, motor, and reward related regions [13][14][15][16][17][18] , and sends output to saccade generating areas in brainstem 19,20 , and has been shown to play important roles in many cognitive processes such as target selection, attention and decision making [21][22][23][24][25][26][27][28][29] . We found that SC neurons encode both absolute value and context-dependent value threshold, suggesting a mechanism that could directly convert absolute values to categorical choice. ...
Value-based decision making involves choosing from multiple options with different values. Despite extensive studies on value representation in various brain regions, the neural mechanism for how multiple value options are converted to motor actions remains unclear. To study this, we developed a multi-value foraging task with varying menu of items in non-human primates using eye movements that dissociates value and choice, and conducted electrophysiological recording in the midbrain superior colliculus (SC). SC neurons encoded “absolute” value, independent of available options, during late fixation. In addition, SC neurons also represent value threshold, modulated by available options, different from conventional motor threshold. Electrical stimulation of SC neurons biased choices in a manner predicted by the difference between the value representation and the value threshold. These results reveal a neural mechanism directly transforming absolute values to categorical choices within SC, supporting highly efficient value-based decision making critical for real-world economic behaviors.
... The core vlPFC regionsthose most consistently included in definitions of the vlPFC across macaque anatomy research groups-are areas 12/47 (rostral and lateral) and 45 [25][26][27][28][29]. In addition, some groups commonly include area 46v [25,[29][30][31], area 12/47O [26,28], and/or area 44 in their definition of vlPFC [11,[32][33][34][35]. Definition of the human vlPFC is more consistent, and typically consists of areas 12/47, 45 and 44 [36,37]. In order to best facilitate future translation to the human, here we define the macaque vlPFC as comprising areas 12/47 (rostral, lateral and orbital), 45 (45A and 45B) and 44. ...
Ventrolateral frontal area 44 is implicated in inhibitory motor functions and facilitating prefrontal control over vocalization. Yet, the corticostriatal circuitry that may contribute to area 44 functions is not clear, as prior investigation of area 44 corticostriatal projections is limited. Here, we used anterograde and retrograde tracing in macaques to map the innervation zone of area 44 corticostriatal projections, quantify their strengths, and evaluate their convergence with corticostriatal projections from non-motor and motor-related frontal regions. First, terminal fields from a rostral area 44 injection site were found primarily in the central caudate nucleus, whereas those from a caudal area 44 injection site were found primarily in the ventrolateral putamen. Second, amongst sampled striatal retrograde injection sites, area 44 input as a percentage of total frontal cortical input was highest in the ventral putamen at the level of the anterior commissure. Third, area 44 projections converged with both orofacial premotor area 6VR and other motor related projections (in the putamen), and with non-motor prefrontal projections (in the caudate nucleus). These findings support the role of area 44 as an interface between motor and non-motor functional domains, possibly facilitated by rostral and caudal area 44 subregions with distinct corticostriatal connectivity profiles.
... The core vlPFC regions-those most consistently included in definitions of the vlPFC across macaque anatomy research groups-are areas 12/47 (rostral and lateral) and 45 (Petrides and Pandya 2002;Romanski 2004Romanski , 2012Saleem et al. 2014;Gerbella et al. 2016). In addition, some groups commonly include area 46v (Price 2008;Borra et al. 2014;Saleem et al. 2014;Gerbella et al. 2016), area 12/47O (Romanski 2004(Romanski , 2012, and/or area 44 in their definition of vlPFC (Petrides 2005;Petrides et al. 2005Petrides et al. , 2012Petrides and Pandya 2009;Saleeba et al. 2019). Definition of the human vlPFC is more consistent and typically consists of areas 12/47, 45, and 44 (Badre and Wagner 2007;Clark et al. 2010). ...
Ventrolateral frontal area 44 is implicated in inhibitory motor functions and facilitating prefrontal control over vocalization. The contribution of corticostriatal circuits to area 44 functions is unclear, as prior investigation of area 44 projections to the striatum-a central structure in motor circuits-is limited. Here, we used anterograde and retrograde tracing in macaques to map the innervation zone of area 44 corticostriatal projections, quantify their strengths, and evaluate their convergence with corticostriatal projections from other frontal cortical regions. First, whereas terminal fields from a rostral area 44 injection site were found primarily in the central caudate nucleus, those from a caudal area 44 injection site were found primarily in the ventrolateral putamen. Second, amongst sampled injection sites, area 44 input as a percentage of total frontal cortical input was highest in the ventral putamen at the level of the anterior commissure. Third, area 44 projections converged with orofacial premotor area 6VR and other motor-related projections (in the putamen), and with nonmotor prefrontal projections (in the caudate nucleus). Findings support the role of area 44 as an interface between motor and nonmotor functional domains, possibly facilitated by rostral and caudal area 44 subregions with distinct corticostriatal connectivity profiles.
