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Journal ArticleDOI

Intracortical and Thalamocortical Connections of the Hand and Face Representations in Somatosensory Area 3b of Macaque Monkeys and Effects of Chronic Spinal Cord Injuries.

30 Sep 2015-The Journal of Neuroscience (Society for Neuroscience)-Vol. 35, Iss: 39, pp 13475-13486
TL;DR: It is shown that reorganization of primary somatosensory area 3b is not accompanied with either an increase in intrinsic cortical connections between the hand and face representations, or any change in thalamocortical inputs to these areas.
Abstract: Brains of adult monkeys with chronic lesions of dorsal columns of spinal cord at cervical levels undergo large-scale reorganization. Reorganization results in expansion of intact chin inputs, which reactivate neurons in the deafferented hand representation in the primary somatosensory cortex (area 3b), ventroposterior nucleus of the thalamus and cuneate nucleus of the brainstem. A likely contributing mechanism for this large-scale plasticity is sprouting of axons across the hand-face border. Here we determined whether such sprouting takes place in area 3b. We first determined the extent of intrinsic corticocortical connectivity between the hand and the face representations in normal area 3b. Small amounts of neuroanatomical tracers were injected in these representations close to the electrophysiologically determined hand-face border. Locations of the labeled neurons were mapped with respect to the detailed electrophysiological somatotopic maps and histologically determined hand-face border revealed in sections of the flattened cortex stained for myelin. Results show that intracortical projections across the hand-face border are few. In monkeys with chronic unilateral lesions of the dorsal columns and expanded chin representation, connections across the hand-face border were not different compared with normal monkeys. Thalamocortical connections from the hand and face representations in the ventroposterior nucleus to area 3b also remained unaltered after injury. The results show that sprouting of intrinsic connections in area 3b or the thalamocortical inputs does not contribute to large-scale cortical plasticity. Significance statement: Long-term injuries to dorsal spinal cord in adult primates result in large-scale somatotopic reorganization due to which chin inputs expand into the deafferented hand region. Reorganization takes place in multiple cortical areas, and thalamic and medullary nuclei. To what extent this brain reorganization due to dorsal column injuries is related to axonal sprouting is not known. Here we show that reorganization of primary somatosensory area 3b is not accompanied with either an increase in intrinsic cortical connections between the hand and face representations, or any change in thalamocortical inputs to these areas. Axonal sprouting that causes reorganization likely takes place at subthalamic levels.
Citations
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Journal ArticleDOI
TL;DR: It is concluded that the cortical representation of the limb remains remarkably stable despite the loss of its main peripheral input and the implications of the stability of sensory representations on the development of upper-limb neuroprostheses.

109 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...In fact, there is little anatomical evidence that the face-elicited activity in SI is mediated by the growth of new cortico-cortical projections: Very few axons cross the face–hand boundary in SI of intact animals (see [57] for analogous results in humans revealed with neuroimaging) and deafferentation of the hand region does not result in any measurable increase in these boundary-crossing projections [58]....

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Journal ArticleDOI
23 Aug 2016-eLife
TL;DR: It is shown that representation of the missing hand’s individual fingers persists in the primary somatosensory cortex even decades after arm amputation, questions the extent to which continued sensory input is necessary to maintain organisation in sensory cortex, thereby reopening the question what happens to a cortical territory once its main input is lost.
Abstract: The hand area of the primary somatosensory cortex contains detailed finger topography, thought to be shaped and maintained by daily life experience. Here we utilise phantom sensations and ultra high-field neuroimaging to uncover preserved, though latent, representation of amputees' missing hand. We show that representation of the missing hand's individual fingers persists in the primary somatosensory cortex even decades after arm amputation. By demonstrating stable topography despite amputation, our finding questions the extent to which continued sensory input is necessary to maintain organisation in sensory cortex, thereby reopening the question what happens to a cortical territory once its main input is lost. The discovery of persistent digit topography of amputees' missing hand could be exploited for the development of intuitive and fine-grained control of neuroprosthetics, requiring neural signals of individual digits.

97 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...…more limited than initially thought, and that instead the functional changes previously observed in S1 following input loss could be attributed to reorganisation in sub-cortical areas in the afferent pathway, principally the brainstem (Jain et al., 1998; Kambi et al., 2014; Chand and Jain, 2015)....

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Journal ArticleDOI
TL;DR: The need to consider potential contributions of additional brain mechanisms, beyond S1 remapping, and the dynamic interplay of contextual factors with brain changes for understanding and alleviating PLP is highlighted.

70 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...It has been suggested that the initial remapping triggered by deprivation will become refined by inputs due to daily hand usage involving compensatory behaviours (Churchill et al., 1998; Elbert et al., 1997)....

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Journal ArticleDOI
TL;DR: The data extend the Brodmann model in human sensorimotor cortex and suggest that body parts are an important organizing principle, similar to the distinction between sensory and motor processing.
Abstract: The cytoarchitectonic map as proposed by Brodmann currently dominates models of human sensorimotor cortical structure, function, and plasticity. According to this model, primary motor cortex, area 4, and primary somatosensory cortex, area 3b, are homogenous areas, with the major division lying between the two. Accumulating empirical and theoretical evidence, however, has begun to question the validity of the Brodmann map for various cortical areas. Here, we combined in vivo cortical myelin mapping with functional connectivity analyses and topographic mapping techniques to reassess the validity of the Brodmann map in human primary sensorimotor cortex. We provide empirical evidence that area 4 and area 3b are not homogenous, but are subdivided into distinct cortical fields, each representing a major body part (the hand and the face). Myelin reductions at the hand-face borders are cortical layer-specific, and coincide with intrinsic functional connectivity borders as defined using large-scale resting state analyses. Our data extend the Brodmann model in human sensorimotor cortex and suggest that body parts are an important organizing principle, similar to the distinction between sensory and motor processing.

63 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...However, a recent definitive study showed that in monkeys with chronic lesions of the dorsal column of spinal cord that had resulted in large-scale map reorganization of hand and face representations in area 3b, nevertheless showed a striking absence of new intracortical projections across the hand–face border (Chand and Jain 2015)....

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Journal ArticleDOI
TL;DR: This review focuses on the reorganization of cortical networks observed after injury and posits a role of intracortical circuits in recovery.

31 citations

References
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Journal Article

4 citations


"Intracortical and Thalamocortical C..." refers background in this paper

  • ...…of brain plasticity is of interest for development of brain– computer interface devices and neuroprostheses because postinjury plasticity can undermine control of devices, or if properly managed, facilitate a better interface (e.g., Enzinger et al., 2008; Jain, 2010; Collignon et al., 2011)....

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