Sensorimotor-independent development of hands and tools selectivity in the visual cortex

Abstract

The visual occipito-temporal cortex is composed of several distinct regions specialized in the identification of different object kinds such as tools and bodies. Its organization appears to reflect not only the visual characteristics of the inputs but also the behavior that can be achieved with them. For example, there are spatially overlapping responses for viewing hands and tools, which is likely due to their common role in object-directed actions. How dependent is occipitotemporal cortex organization on object manipulation and motor experience? To investigate this question, we studied five individuals born without hands (individuals with upper limb dysplasia), who use tools with their feet. Using fMRI, we found the typical selective hand-tool overlap (HTO) not only in typically developed control participants but also in four of the five dysplasics. Functional connectivity of the HTO in the dysplasics also showed a largely similar pattern as in the controls. The preservation of functional organization in the dysplasics suggests that occipito-temporal cortex specialization is driven largely by inherited connectivity constraints that do not require sensorimotor experience. These findings complement discoveries of intact functional organization of the occipito-temporal cortex in people born blind, supporting an organization largely independent of any one specific sensory or motor experience.T he visual occipito-temporal cortex contains multiple domainsensitive regions (1) that are highly reproducible across individuals. Much is known about these regions' large-scale organization. Consistent with the patterns of neuropsychological dissociations showing a fundamental distinction between animate and inanimate objects (2, 3), neuroimaging results have shown that the animate/ inanimate distinction is the primary organizational dimension in the occipito-temporal cortex (4-8), with a secondary distinction within the inanimate domain between navigation-relevant (e.g., large nonmanipulable objects and scenes) and small, manipulable inanimate objects (9-12). What are the principles that guide this organization? One possibility is that it is the direct result of experience, critically dependent on the individual's life experiences and expertise (13)(14)(15)(16)(17)). An alternative is that experience merely modulates an already existing innately determined structure, driven by connectivity constraints (4, 18-21) between regions within the occipito-temporal cortex and downstream areas specialized in processing specific object types.A notable example supporting the close link between visual form processing and its downstream use is a specific region in the occipito-temporal cortex that shows spatially overlapping preferences for hands and tools (22,23). This overlapping specialization is obviously not based on visual similarity alone because hands and tools are visually quite distinct. Nor is it due to general domain specialization because animate and inanimate objects are otherwise distinct (24-26). Instead, the overlap may ...

Large-scale organization of the hand action observation network in individuals born without hands

“…No participant had a history of psychiatric or neurological disorder. All the IDs had developed fine motor skills of the feet and used their feet for many typical hand-related actions of daily life (e.g., opening or closing doors; for more information about IDs' foot use see Vannuscorps et al 2014;Striem-Amit et al 2017) and none had history of phantom limb sensations or movements (tested as in Vannuscorps and Caramazza 2016). Two TDs were excluded from the sample due to poor behavioral performance (error rate exceeding the group mean by > 2 SDs) in the experimental task.…”

“…In favor of a critical role for experience, it has been shown that the emergence of the brain's typical area of specialization for letters requires reading experience (Baker et al 2007;Dehaene et al 2010;Saygin et al 2016). By contrast, the neural representation of tools and hands appears to be virtually the same in congenitally blind individuals Kitada et al 2014;Striem-Amit and Amedi 2014), individuals born without hands (Striem-Amit et al 2017), and in the typically developed population (Bracci et al 2012). Here, we investigated the role of sensorimotor experience in shaping the organization of the action observation network as a window on this question.…”

Consensus Paper: Cerebellum and Social Cognition

“…The purpose of this article is to offer further support for a cerebellum-driven social learning explanation of the evolution of stone-tool making. This additional support is based on the findings of the existence of (1) an innate hand-tool overlap in the cerebrum [ 55 ] and (2) specific tool modules in the lateral posterior cerebellum for both actual and imagined tool use [ 56 , 57 ].…”

“…The cerebellum’s dentate nucleus sends both actual tool use and imaginary tool use models to the cerebral cortex where they can be consciously experienced [ 58 ] . Second , in studying dysplasics (individuals born without hands), Striem-Amit, Vannuscope, and Caramazza [ 55 ] have described the evolution of an innate hand-tool overlap area in the occipital–temporal area of the cerebral cortex for the acceptance of tools into the hand: The hand tool overlap would have emerged because of the potential advantage that accrues from the efficient processing of hands and tools as parts of a common (or closely intertwined), specialized system [tools being advantageous ancillaries. This system, in turn, is connected to the dorsal, action-processing areas [parietal cortex] to allow quick and efficient shaping of hands to grasp and use tools [requiring both phylogenetic and ontogenetic cerebellar refinement].…”

Brain Plasticity: When the Feet and Mouth Replace the Hand

“…Since such task-directed organization in the visual cortex is found in people born blind, it cannot be based on visual experience alone. Furthermore, it is likely not based on one's sensory or motor experience alone, as visual handselectivity patterns are also found in people born without hands [12]. Support for this model has also been provided from the auditory cortex, showing task-specificity from other senses in deafness [13,14].…”