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Comparisons across adults with different sensory histories (blind vs. sighted) have uncovered effects of experience on the development of human brain function. In people born blind visual cortices become responsive to non-visual tasks and show enhanced functional coupling with fronto-parietal executive systems at rest. Little is known about the developmental origins of experience-based plasticity in humans, since almost all research has been done with adults. Here we take a new approach by comparing resting state data across blind (n=30) and blindfolded sighted (n=50) adults to two large cohorts of sighted infants (dHCP, n=327, n=475). By comparing the infant “starting state” to adult outcomes, we dissociate the instructive role of vision from reorganization due to blindness. As previously reported, we find that in sighted adults, visual networks show stronger functional coupling with other sensory-motor networks (i.e., auditory, somatosensory) than with higher-cognitive prefrontal networks at rest. By contrast, visual cortices of adults born blind show the opposite pattern: stronger functional connectivity with higher-cognitive prefrontal networks. Remarkably, we find that the connectivity profile of secondary visual cortices in infants resembles that of blind more than sighted adults. Visual experience appears to ‘instruct’ coupling of visual cortex with other sensory-motor networks and de-couple from prefrontal systems. By contrast primary visual cortex (V1) shows a mixture of instructive effects of vision and reorganizing effects of blindness. Finally, lateralization of occipital connectivity appears to be driven by blindness-related reorganization, since infants resembles sighted adults. These results reveal instructive and reorganizing effect of experience on functional connectivity of human cortex.

How do life experiences impact cortical function? In people who are born blind, the “visual” cortices are recruited for nonvisual tasks such as Braille reading and sound localization (e.g., Collignon et al., 2011; Sadato et al., 1996). The mechanisms of this recruitment are not known. Do visual cortices have a latent capacity to respond to nonvisual information that is equal throughout the lifespan? Alternatively, is there a sensitive period of heightened plasticity that makes visual cortex repurposing possible during childhood? To gain insight into these questions, we leveraged naturalistic auditory stimuli to quantify and compare cross-modal responses congenitally blind (CB, n=22), adult-onset blind (vision loss >18 years-of-age, AB, n=14) and sighted (n=22) individuals. Participants listened to auditory excerpts from movies; a spoken narrative; and matched meaningless auditory stimuli (i.e., shuffled sentences, backwards speech) during fMRI scanning. These rich naturalistic stimuli made it possible to simultaneous engage a broad range of cognitive domains. We correlated the voxel-wise timecourses of different participants within each group. For all groups, all stimulus conditions induced synchrony in auditory cortex and for all groups only the narrative stimuli synchronized responses in higher-cognitive fronto-parietal and temporal regions. Inter-subject synchrony in visual cortices was high in the CB group for the movie and narrative stimuli but not for meaningless auditory controls. In contrast, visual cortex synchrony was equally low among AB and sighted blindfolded participants. Even many years of blindness in adulthood fail to enable responses to naturalistic auditory information in visual cortices of people who had sight as children. These findings suggest that cross-modal responses in visual cortex of people born blind reflect the plasticity of developing visual cortex during a sensitive period.

We rely upon visual short-term memory (VSTM) for continued access to perceptual information that is no longer available. Despite the complexity of our visual environments, the majority of research on VSTM has focused on memory for lower-level perceptual features. Using more naturalistic stimuli, it has been found that recognizable objects are remembered better than unrecognizable objects. What remains unclear, however, is how semantic information changes brain representations in order to facilitate this improvement in VSTM for real-world objects. To address this question, we used a continuous report paradigm to assess VSTM (precision and guessing rate) while participants underwent functional magnetic resonance imaging (fMRI) to measure the underlying neural representation of 96 objects from 4 animate and 4 inanimate categories. To isolate semantic content, we used a novel image generation method that parametrically warps images until they are no longer recognizable while preserving basic visual properties. We found that intact objects were remembered with greater precision and a lower guessing rate than unrecognizable objects (this also emerged when objects were grouped by category and animacy). Representational similarity analysis of the ventral visual stream found evidence of category and animacy information in anterior visual areas during encoding only, but not during maintenance. These results suggest that the effect of semantic information during encoding in ventral visual areas boosts visual short-term memory for real-world objects.

The development of the ventral visual stream is shaped both by an innate proto-organization and by experience. The fusiform face area (FFA), for example, has stronger connectivity to early visual regions representing the fovea and lower spatial frequencies. In adults, category-selective regions in the ventral stream (e.g. the FFA) also have distinct signatures of connectivity to widely distributed brain regions, which are thought to encode rich cross-modal, motoric, and affective associations (e.g., tool regions to the motor cortex). It is unclear whether this long-range connectivity is also innate, or if it develops with experience. We used MRI diffusion-weighted imaging with tractography to characterize the connectivity of face, place, and tool category-selective regions in neonates (N=445), 1-9 month old infants (N=11), and adults (N=14). Using a set of linear-discriminant classifiers, category-selective connectivity was found to be both innate and shaped by experience. Connectivity for faces was the most developed, with no evidence of significant change in the time period studied. Place and tool networks were present at birth but also demonstrated evidence of development with experience, with tool connectivity developing over a more protracted period (9 months). Taken together, the results support an extended proto-organizon to include long-range connectivity that could provide additional constraints on experience dependent development.

Identifying what an object is, and whether an object has been encountered before, is a crucial aspect of human behavior. Despite this importance, we do not have a complete understanding of the neural basis of these abilities. Investigations into the neural organization of human object representations have revealed category specific organization in the ventral visual stream in perceptual tasks. Interestingly, these categories fall within broader domains of organization, with distinctions between animate, inanimate large, and inanimate small objects. While there is some evidence for category specific effects in the medial temporal lobe (MTL), it is currently unclear whether domain level organization is also present across these structures. To this end, we used fMRI with a continuous recognition memory task. Stimuli were images of objects from several different categories, which were either animate or inanimate, or large or small within the inanimate domain. We employed representational similarity analysis (RSA) to test the hypothesis that object-evoked responses in MTL structures during recognition-memory judgments also show evidence for domain-level organization along both dimensions. Our data support this hypothesis. Specifically, object representations were shaped by either animacy, real-world size, or both, in perirhinal and parahippocampal cortex, as well as the hippocampus. While sensitivity to these dimensions differed when structures when probed individually, hinting at interesting links to functional differentiation, similarities in organization across MTL structures were more prominent overall. These results argue for continuity in the organization of object representations in the ventral visual stream and the MTL.

ObjectiveFunctional connectivity magnetic resonance imaging (fcMRI) of neonates with perinatal brain injury could improve prediction of motor impairment before symptoms manifest, and establish how early brain organization relates to subsequent development. Methods: This cohort study is the first to describe and quantitatively assess functional brain networks and their relation to later motor skills in neonates with a diverse range of perinatal brain injuries. Infants (n=65, included in final analyses: n=53) were recruited from the neonatal intensive care unit (NICU) and were stratified based on their age at birth (premature vs. term), and on whether neuropathology was diagnosed from structural MRI. Functional brain networks and a measure of disruption to functional connectivity were obtained from 14 minutes of fcMRI acquired during natural sleep at term-equivalent age.ResultsDisruption to connectivity of the somatomotor and frontoparietal executive networks predicted motor impairment at 4 and 8 months. This disruption in functional connectivity was not found to be driven by differences between clinical groups, or by any of the specific measures we captured to describe the clinical course.ConclusionfcMRI was predictive over and above other clinical measures available at discharge from the NICU, including structural MRI. Motor learning was affected by disruption to somatomotor networks, but also frontoparietal executive networks, which supports the functional importance of these networks in early development. Disruption to these two networks might be best addressed by distinct intervention strategies.

AimHead motion has a profound effect on MRI, and will contaminate comparisons of function or structure between groups that move differently. This work compares adults and infants. Infants might move differently for physical, physiological and cognitive reasons, but so far these differences have not been quantified.MethodsThe spatial modes and total magnitude of motion in the MRI scanner were measured (N=211). The effects of group (infant vs. adult) and stimulation paradigm (auditory vs. visual) were evaluated.ResultsSpatial modes of motion were found to be distinct between infant and adult groups. Infants had less anterior-posterior translational motion, but greater motion in other dimensions, often with complex multi-axis patterns. In magnitude distribution, sleeping infants often remained more still than adults, but when movement did occur it was more extreme and abrupt. Two groups of adults presented with different stimulation showed similar shapes of motion.ConclusionThe spatial modes and magnitude distribution of motion differed substantially between groups, and must be considered carefully as a confound in comparisons of structure or function. The abruptness and magnitude of movement suggests that for infants relative to adults post-processing strategies such as de-noising are likely to be more effective than prospective motion correction.Key notesQuantified the spatial and temporal distribution of motion during MRI in 211 adults and neonatesThe different spatial modes in adults and infants were visualized and statistically contrastedThe magnitude of motion had “heavier tails” in infants, with more still periods, and more large movements, than adults.