A hierarchical, retinotopic proto-organization of the primate visual system at birth

Arcaro, Michael; Livingstone, Margaret S.

doi:10.7554/elife.26196

Cited by 201 publications

(191 citation statements)

References 81 publications

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“…We speculate that the early somatotopic organization observed in newborn monkeys provides the scaffolding for the subsequent development of these functional domains. This organization parallels our recent findings that the entire visual system is retinotopically organized at birth 47 and likely supports experience-driven development of behaviorally relevant domains, such as those that selectively respond to text or faces 48 . Together, these findings illustrate that topographic maps of sensory space are a fundamental and pervasive ( Figure 8) organizing principle of the brain, and they play an important role in development by guiding and constraining experience-driven refinement and specialization.…”

Section: Discussionsupporting

confidence: 88%

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Body-map proto-organization in newborn macaques

Arcaro

Schade

Livingstone

2019

Preprint

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Topographic sensory maps are a prominent feature of the adult primate brain. Here, we asked whether topographic representations of the environment are fundamental to early development. Using fMRI, we find that the newborn somato-motor system, spanning frontoparietal cortex and subcortex, comprises multiple topographic body representations. The organization of these large-scale body maps was indistinguishable from those in adults and already exhibited features stereotypical of adult maps. Finer-scale differentiation of individual fingers increased over the first two years, suggesting that topographic representations are refined during early development. Last, we found that somato-motor representations were unchanged in two visually impaired monkeys who relied entirely on touch for interacting with their environment, demonstrating that massive shifts in early sensory experience in an otherwise anatomically intact brain are not sufficient for driving cross-modal plasticity. We propose that a topographic scaffolding is present at birth that both directs and constrains experience-driven modifications throughout sensory systems.

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Section: Discussionsupporting

confidence: 88%

“…As illustrated by a group average (n = 8) body map, anterior parietal and frontal cortex comprise somatotopic representations of the body. These retinotopic 47 and somatotopic maps (current study) are present at birth. Black dashed lines differentiate retinotopic and somatotopic maps.…”

Section: Discussionsupporting

confidence: 56%

Body-map proto-organization in newborn macaques

Arcaro

Schade

Livingstone

2019

Preprint

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“…In fact, the functional organization of occipital regions has been thought to develop based on innate protomaps implementing computational bias for low-level visual features including retinal eccentricity bias , orientation content (Rice, Watson, Hartley, & Andrews, 2014), spatial frequency content (Rajimehr, Devaney, Bilenko, Young, & Tootell, 2011) and the average curvilinearity/rectilinearity of stimuli (Nasr, Echavarria, & Tootell, 2014). This proto-organization would serve as low-level visual biases scaffolding experience-dependent domain specialization (Arcaro & Livingstone, 2017;Gomez, Barnett, & Grill-Spector, 2019). Consequently, in absence of visual experience, the functional organization of the occipital cortex cannot develop according to this proto-organization and those regions may therefore switch their functional tuning toward distant computations (Bedny, 2017).…”

Section: Introductionmentioning

confidence: 99%

Categorical representation from sound and sight in the ventral occipito-temporal cortex of sighted and blind

Mattioni

Rezk

Battal

et al. 2019

Preprint

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and Olivier Collignon (olivier.collignon@uclouvain.be). AbstractThe Ventral Occipito-Temporal Cortex (VOTC) shows reliable category selective response to visual information. Do the development, topography and information content of this categorical organization depend on visual input or even visual experience? To further address this question, we used fMRI to characterize the brain responses to eight categories (4 living, 4 non-living) presented acoustically in sighted and early blind individuals, and visually in a separate sighted group. Using a combination of decoding and representational similarity analyses, we observed that VOTC reliably encodes sounds categories in the sighted and blind groups, using a representational structure strikingly similar to the one found in vision. Moreover, we found that the representational connectivity between VOTC and large-scale brain networks was substantially similar across modalities and groups. Blind people however showed higher decoding accuracies and higher inter-subject consistency for the representation of sounds in VOTC, and the correlation between the representational structure of visual and auditory categories was almost double in the blind when compared to the sighted group. Crucially, we also demonstrate that VOTC represents the categorical membership of sounds rather that their acoustic features in both groups. Our results suggest that early visual deprivation triggers an extension of the intrinsic categorical organization of VOTC that is at least partially independent from vision.

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“…Further, the comparison between adults and neonates shows significant differences between groups to all networks except the SM network, and only marginally significant differences between groups in the Vis and DA networks. The similarity between adults and neonates in connectivity to the SM and Vis networks may be due to the relative maturity of these areas at birth (Arcaro & Livingstone, 2017;Deen et al, 2017;Hurk et al, 2017;Gao et al 2017, Dall'Orso et al, 2018.…”

Section: Discussionmentioning

confidence: 99%

The intrinsic neonatal hippocampal network: rsfMRI findings

Howell

Osher

Saygin

2019

Preprint

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Many adults cannot voluntarily recall memories before the ages of 3-5, a phenomenon referred to as "infantile amnesia". The development of the hippocampal network likely plays a significant part in the emergence of the ability to form long-lasting memories. In adults, the hippocampus has specialized and privileged connections with certain cortical networks, which presumably facilitate its involvement in memory encoding, consolidation, and retrieval. Is the hippocampus already specialized in these cortical connections at birth? And are the topographical principles of connectivity (e.g. long-axis specialization) present at birth? We analyzed resting-state hippocampal connectivity in neonates scanned within one week of birth (Developmental Human Connectome Project) and compared them to adults (Human Connectome Project). We explored the connections of the whole hippocampus and its long-axis specialization to seven canonical cortical networks. We found that the neonatal hippocampal networks show clear immaturity at birth: adults showed hippocampal connectivity that was unique for each cortical network, whereas neonates showed no differentiation in hippocampal connectivity across these networks. Further, neonates lacked long-axis specialization (i.e., along anterior-posterior axis) of the hippocampus in its differential connectivity patterns to the cortical networks. This immaturity in connectivity may contribute to immaturity in memory formation in the first years of life. Significance Statement:While animal data, and anatomical and behavioral human data from young children suggest that the hippocampus is immature at birth, to date, there are no direct assessments of human hippocampal functional connectivity (FC) very early in life. Our study explores the FC of the hippocampus to the cortex at birth, allowing insight into the development of human memory systems.Recently, Wael and colleagues (2018) showed the hippocampus has a clear intrinsic pattern of functional connectivity (FC) to a set of cortical networks in adults. Further, this connectivity pattern differed between the anterior and posterior portions of the hippocampus. This so-called long-axis specialization of the hippocampus is consistent with previous research showing that the anterior and posterior hippocampus display different patterns of structural and functional connectivity and may be uniquely activated in response to cognitive, memory and spatial demands (for reviews see Poppenk et al., 2013, Strange et al., 2014. The development of the hippocampal

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A hierarchical, retinotopic proto-organization of the primate visual system at birth

Cited by 201 publications

References 81 publications

Body-map proto-organization in newborn macaques

Body-map proto-organization in newborn macaques

Categorical representation from sound and sight in the ventral occipito-temporal cortex of sighted and blind

The intrinsic neonatal hippocampal network: rsfMRI findings

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