Sensitive periods for the functional specialization of the neural system for human face processing

Röder, Brigitte; Ley, Pia; Shenoy, Bhamy Hariprasad; Kekunnaya, Ramesh; Bottari, Davide

doi:10.1073/pnas.1309963110

Cited by 80 publications

(76 citation statements)

References 33 publications

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“…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)(19)(20)(21) between regions within the occipito-temporal cortex and downstream areas specialized in processing specific object types.…”

mentioning

confidence: 99%

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

Striem-Amit

Vannuscorps

Caramazza

2017

Proc. Natl. Acad. Sci. U.S.A.

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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 ...

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confidence: 99%

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

Striem-Amit

Vannuscorps

Caramazza

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Individual case studies suggest early visual deprivation impairs object as well as face recognition abilities (20)(21)(22)(23)(24). Furthermore, such deprivation has been shown to compromise electrophysiological components believed to be associated with face perception (25). Even relatively short periods of deprivation ranging in duration from 2 to 6 mo after birth have been shown to have significant detrimental consequences on face recognition skills.…”

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confidence: 99%

Emergence of categorical face perception after extended early-onset blindness

Gandhi

Singh

Swami

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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It is unknown whether the ability to visually distinguish between faces and nonfaces is subject to a critical period during development. Would a congenitally blind child who gains sight several years after birth be able to acquire this skill? This question has remained unanswered because of the rarity of cases of late sight onset. We had the opportunity to work with five early-blind individuals who gained sight late in childhood after treatment for dense bilateral cataracts. We tested their ability to categorize patterns as faces, using natural images that spanned a spectrum of face semblance. The results show that newly sighted individuals are unable to distinguish between faces and nonfaces immediately after sight onset, but improve markedly in the following months. These results demonstrate preserved plasticity for acquiring face/ nonface categorization ability even late in life, and set the stage for investigating the informational and neural basis of this skill acquisition.face classification | blindness | visual learning | sight restoration | plasticity

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“…In the present context, the lack of N170 tuning in congenital cataract participants would typically evoke a "pruning" explanation: a failure to eliminate incorrect synapses. Eschewing such simplistic explanations, Röder et al (5) suggest that the lack of tuning is because of the failure of inhibitory processes to be shaped by experience. This idea is consistent with the well-established mechanisms that underlie critical period visual plasticity and tuning in animal models (17).…”

Section: Mechanisms: Tuning or Pruning?mentioning

confidence: 99%

“…By the clever juxtaposition of two clinical populations with restored vision-those who had congenital cataracts versus those whose cataracts developed postnatally-Röder et al (5) demonstrate the existence of a sensitive period for the tuning of a face-sensitive neural response in humans. The exact time at which visual experience is necessary for face-specificity remains unknown and could not be addressed in this study because of the varied timing of sight restoration (and thus the amount of visual experience) of each clinical participant.…”

Section: Mechanisms: Tuning or Pruning?mentioning

confidence: 99%

“…Part of the problem, of course, is that one cannot do perturbation experiments in humans as we would with an animal model system (4). A new electrophysiology study by Röder et al (5) capitalizes on a naturally occurring experiment: a unique clinical population of individuals born blind because of cataracts, who then later have their sight restored following cataract removal (5). The study revealed that the neural signature for face processing is present in these individuals but not sufficiently tuned by experience.…”

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confidence: 99%

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