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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: This article is aimed at providing a comprehensive understanding of central nervous system plasticity involving peripheral nerve injury by reviewing studies mainly in human or nonhuman primate and by highlighting the functional and structural modifications in thecentral nervous system after peripheral nerve transfer.
Abstract: Peripheral nerve injury can lead to partial or complete loss of limb function, and nerve transfer is an effective surgical salvage for patients with these injuries. The inability of deprived cortical regions representing damaged nerves to overcome corresponding maladaptive plasticity after the reinnervation of muscle fibers and sensory receptors is thought to be correlated with lasting and unfavorable functional recovery. However, the concept of central nervous system plasticity is rarely elucidated in classical textbooks involving peripheral nerve injury, let alone peripheral nerve transfer. This article is aimed at providing a comprehensive understanding of central nervous system plasticity involving peripheral nerve injury by reviewing studies mainly in human or nonhuman primate and by highlighting the functional and structural modifications in the central nervous system after peripheral nerve transfer. Hopefully, it will help surgeons perform successful nerve transfer under the guidance of modern concepts in neuroplasticity.

3 citations

Posted ContentDOI
31 Aug 2020-bioRxiv
TL;DR: It is shown that in area 3b of macaque monkeys, most neurons in the thumb representation do not respond to tactile stimulation of other digits and receive few intrinsic cortical inputs from other digits, whereas there is significantly more inter-digital information exchange between the other digits.
Abstract: The evolution of opposable thumb has enabled fine grasping ability and precision grip, which led to the capacity for fine manipulation of objects and refined tool use. Since tactile inputs to an opposable thumb are often spatially and temporally out of synch with inputs from the fingers, we hypothesized that inputs from the opposable thumb would be processed in an independent module in the primary somatosensory cortex (area 3b). Here we show that in area 3b of macaque monkeys, most neurons in the thumb representation do not respond to tactile stimulation of other digits and receive few intrinsic cortical inputs from other digits. However, neurons in the representations of other digits respond to touch on any of the four digits and are significantly more interconnected in the cortex. The thumb inputs are thus processed in an independent module, whereas there is significantly more inter-digital information exchange between the other digits. This cortical organization reflects behavioral use of the hand with an opposable thumb.

2 citations


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

  • ...…of all the digits in area 3b of macaque monkeys, there are no differences in the density of Meissner’s corpuscles, tactile sensitivity, or receptive field sizes of neurons between the thumb and other digits (Chand and Jain 2015; Verendeev et al. 2015; Sathian and Zangaladze 1996; Sur et al. 1980)....

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  • ...A second series of sections were stained for myelin using a modified Gallyas procedure (Jain et al. 1998) to visualize area 3b, the hand-face border, and the inter-digit borders (Chand and Jain 2015)....

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  • ...6; Jain et al. 1998), which we have previously shown to reveal anatomical borders between the digits, and between D1 and the face representations (Chand and Jain 2015)....

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  • ...Only neurons determined to be in the hand representation of area 3b were considered for quantitative analysis (Chand and Jain 2015)....

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  • ...1998) to visualize area 3b, the hand-face border, and the inter-digit borders (Chand and Jain 2015)....

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Posted ContentDOI
29 Jul 2020-bioRxiv
TL;DR: In the human posterior parietal cortex (PPC), single units encode high-dimensional information with partially mixed representations that enable small populations of neurons to encode many variables relevant to movement planning, execution, cognition, and perception as discussed by the authors.
Abstract: In the human posterior parietal cortex (PPC), single units encode high-dimensional information with partially mixed representations that enable small populations of neurons to encode many variables relevant to movement planning, execution, cognition, and perception. Here we test whether a PPC neuronal population previously demonstrated to encode visual and motor information is similarly selective in the somatosensory domain. We recorded from 1423 neurons within the PPC of a human clinical trial participant during objective touch presentation and during tactile imagery. Neurons encoded experienced touch with bilateral receptive fields, organized by body part, and covered all tested regions. Tactile imagery evoked body part specific responses that shared a neural substrate with experienced touch. Our results are the first neuron level evidence of touch encoding in human PPC and its cognitive engagement during tactile imagery which may reflect semantic processing, sensory anticipation, and imagined touch.

1 citations

Journal ArticleDOI
TL;DR: Brodmann’s area maps were proved to be a useful functional atlas for cortical localization of tactile perception evoked by fabric touch and showed that activation information in the participants’ brain can distinguish the fabric samples very well.
Abstract: Different sensations are generated when we touch textiles with different performance. The mechanical properties related to fabric touch have been studied for a long time, the relationship between which and the subjective feelings is well understood. However, the cognitive mechanism of our brain on the tactile perception evoked by fabric touch were rarely studied. The relationship between mechanical properties of fabrics and the brain response in different areas is the vacancy of the study but urgent problem. In our previous study, the advanced technology of fMRI was proved to be an effective tool for detecting brain response evoked by tactile stimulation of fabric touch with high spatial resolution. Now in this study, further fMRI experiments were conducted to observe brain response when participants touched different fabrics using their fingers in a specified way, and the most widely recognized functional atlas, Brodmann’s area maps, were applied to locate the cortical activations in functional areas. Activations in the participants’s brain in different Brodmann areas was compared with the mechanical preperties of the fabric samples tested by the instruments of KES-FB. The results showed that activation information in the participants’ brain can distinguish the fabric samples very well. Activations in several Brodmann areas are closely connected with different tactile preperties of the fabrics. Therefore, Brodmann’s area maps were proved to be a useful functional atlas for cortical localization of tactile perception evoked by fabric touch.
Journal ArticleDOI
TL;DR: In this article, the authors studied how local circuitries within each layer of the deafferented cortex set the basis for neuroplastic changes after immediate thoracic spinal cord injury (SCI) in anaesthetised rats.
Abstract: Sensory stimulation of forelimb produces cortical evoked responses in the somatosensory hindlimb cortex in a layer-dependent manner Spinal cord injury favours the input statistics of cortico-cortical connections between intact and deafferented cortices After spinal cord injury supragranular layers exhibit better integration of spontaneous of corticocortical information while infragranular layers exhibit better integration of evoked sensory stimulation Cortical reorganization is a layer-specific phenomenon ABSTRACT: Cortical areas have the capacity of large-scale reorganization following sensory deafferentation. However, it remains unclear whether this phenomenon is a unique process that homogenously affects an entire deprived cortical region or it is suitable to changes depending on neuronal networks across distinct cortical layers. Here, we studied how local circuitries within each layer of the deafferented cortex set the basis for neuroplastic changes after immediate thoracic spinal cord injury (SCI) in anaesthetised rats. In vivo electrophysiological recordings from deafferented hindlimb somatosensory cortex showed that SCI induces layer-specific changes mediating evoked and spontaneous activity. In supragranular layers 2/3, SCI increased gamma oscillations and the ability of these neurons to initiate up-states during spontaneous activity, suggesting altered corticocortical network and/or intrinsic properties that may serve to maintain the excitability of the cortical column after deafferentation. On the other hand, SCI enhanced infragranular layers' ability to integrate evoked-sensory inputs leading to increased and faster neuronal responses. Delayed evoked-responses onset were also observed in layers 5/6, suggesting alterations in thalamocortical connectivity. Altogether, our data indicate that SCI immediately modifies local circuitries within the deafferented cortex allowing supragranular layers to better integrate spontaneous corticocortical information, and thus modifying column excitability, and infragranular layers to better integrate evoked-sensory inputs to preserve subcortical outputs. These layer-specific neuronal changes may guide the long-term alterations in neuronal excitability and plasticity associated to the rearrangements of somatosensory networks and the appearance of central sensory pathologies usually associated with spinal cord injury. This article is protected by copyright. All rights reserved.
References
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Journal ArticleDOI
TL;DR: The results indicated that the deprivation caused by monocular suture produced a decrease in the cytochrome oxidase staining of the binocular segment of the deprived geniculate laminae of kittens, leading to a significant decreases in the level of oxidative enzyme activity one to several synapses away.

1,862 citations


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

  • ...Other series of sections were stained for cytochrome oxidase (CO) (Wong-Riley, 1979), Nissl substance and AChE (Mohammed and Jain, 2014)....

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Journal ArticleDOI
28 Jun 1991-Science
TL;DR: The results show the need for a reevaluation of both the upper limit of cortical reorganization in adult primates and the mechanisms responsible for it.
Abstract: After limited sensory deafferentations in adult primates, somatosensory cortical maps reorganize over a distance of 1 to 2 millimeters mediolaterally, that is, in the dimension along which different body parts are represented. This amount of reorganization was considered to be an upper limit imposed by the size of the projection zones of individual thalamocortical axons, which typically also extend a mediolateral distance of 1 to 2 millimeters. However, after extensive long-term deafferentations in adult primates, changes in cortical maps were found to be an order of magnitude greater than those previously described. These results show the need for a reevaluation of both the upper limit of cortical reorganization in adult primates and the mechanisms responsible for it.

1,051 citations


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

  • ...…such as transection of the dorsal columns (10 –14 mm, and sometimes more that 20 mm, Jain et al., 2008) or transection of dorsal roots (Pons et al., 1991), is beyond what can be mediated by normal connections in the brain, reorganization must involve axonal sprouting (Kaas et al.,…...

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  • ...We extend these observations and show that chin representation also has only few connections across the hand– face border, which is important because it is the chin representation that expands as a result of massive deafferentations (Pons et al., 1991; Jain et al., 1997, 2008)....

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  • ...…at multiple sites along the somatosensory pathway, it has been proposed that reorganization could take place at all these sites independently, or changes at upstream areas could be a reflection of the downstream reorganization (Pons et al., 1991; Kaas et al., 1999; Jones, 2000; Kambi et al., 2014)....

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  • ...Similar reorganization in area 3b is also seen in monkeys with chronic transection of the dorsal roots from C2 to T4 (Pons et al., 1991)....

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Journal ArticleDOI
TL;DR: The results suggest that M1 injury results in axonal sprouting near the ischemic injury and the establishment of novel connections within a distant target, and support the hypothesis that, after a cortical injury, such as occurs after stroke, cortical areas distant from the injury undergo major neuroanatomical reorganization.
Abstract: Previously, we showed that the ventral premotor cortex (PMv) underwent neurophysiological remodeling after injury to the primary motor cortex (M1). In the present study, we examined cortical connections of PMv after such lesions. The neuroanatomical tract tracer biotinylated dextran amine was injected into the PMv hand area at least 5 months after ischemic injury to the M1 hand area. Comparison of labeling patterns between experimental and control animals demonstrated extensive proliferation of novel PMv terminal fields and the appearance of retrogradely labeled cell bodies within area 1/2 of the primary somatosensory cortex after M1 injury. Furthermore, evidence was found for alterations in the trajectory of PMv intracortical axons near the site of the lesion. The results suggest that M1 injury results in axonal sprouting near the ischemic injury and the establishment of novel connections within a distant target. These results support the hypothesis that, after a cortical injury, such as occurs after stroke, cortical areas distant from the injury undergo major neuroanatomical reorganization. Our results reveal an extraordinary anatomical rewiring capacity in the adult CNS after injury that may potentially play a role in recovery.

665 citations


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

  • ...tral premotor cortex after M1 lesions (Dancause et al., 2005)....

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  • ...Axonal sprouting in the cortex has been reported following limb amputations (Florence et al., 1998), focal retinal lesions (Darian-Smith and Gilbert, 1994), and cortical injuries (Dancause et al., 2005)....

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  • ...And in the motor cortex of adult squirrel monkeys, novel terminal fields were observed in ventral premotor cortex after M1 lesions (Dancause et al., 2005)....

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  • ..., 1998), focal retinal lesions (Darian-Smith and Gilbert, 1994), and cortical injuries (Dancause et al., 2005)....

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  • ...…between the hand and the face representations appears to be a strong limiting boundary that does not permit sprouting across, unlike that seen within the hand representation or other cortical areas following injuries (Darian-Smith and Gilbert, 1994; Florence et al., 1998; Dancause et al., 2005)....

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Journal ArticleDOI
21 Apr 1994-Nature
TL;DR: It is reported here that structural changes in the form of axonal sprouting of long-range laterally projecting neurons accompany topographic remodelling of the visual cortex.
Abstract: Removal of sensory input from a focal region of adult neocortex can lead to a large reorganization of cortical topography within the deprived area during subsequent months. Although this form of functional recovery is now well documented across several sensory systems, the underlying cellular mechanisms remain elusive. Weeks after binocular retinal lesions silence a corresponding portion of striate cortex in the adult cat, this cortex again becomes responsive, this time to retinal loci immediately outside the scotoma. Earlier findings showed a lack of reorganization in the lateral geniculate nucleus and an inadequate spread of geniculocortical afferents to account for the cortical reorganization, suggesting the involvement of intrinsic cortical connections. We investigated the possibility that intracortical axonal sprouting mediates long-term reorganization of cortical functional architecture. The anterograde label biocytin was used to compare the density of lateral projections into reorganized and non-deprived cortex. We report here that structural changes in the form of axonal sprouting of long-range laterally projecting neurons accompany topographic remodelling of the visual cortex.

608 citations


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

  • ...Axonal sprouting in the cortex has been reported following limb amputations (Florence et al., 1998), focal retinal lesions (Darian-Smith and Gilbert, 1994), and cortical injuries (Dancause et al., 2005)....

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  • ...Sprouting was also seen in the primary visual cortex of animals with retinal lesions (Darian-Smith and Gilbert, 1994; Yamahachi et al., 2009)....

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  • ...…between the hand and the face representations appears to be a strong limiting boundary that does not permit sprouting across, unlike that seen within the hand representation or other cortical areas following injuries (Darian-Smith and Gilbert, 1994; Florence et al., 1998; Dancause et al., 2005)....

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Journal ArticleDOI
20 Apr 2000-Nature
TL;DR: In ferrets in which retinal projections are routed into the auditory pathway, visually responsive neurons in ‘rewired’ primary auditory cortex are also organized into orientation modules, showing that afferent activity has a profound influence on diverse components of cortical circuitry, including thalamocortical and local intracortical connections, which are involved in the generation of orientation tuning, and long-range horizontal connections which are important in creating an orientation map.
Abstract: Modules of neurons sharing a common property are a basic organizational feature of mammalian sensory cortex. Primary visual cortex (V1) is characterized by orientation modules—groups of cells that share a preferred stimulus orientation—which are organized into a highly ordered orientation map. Here we show that in ferrets in which retinal projections are routed into the auditory pathway, visually responsive neurons in ‘rewired’ primary auditory cortex are also organized into orientation modules. The orientation tuning of neurons within these modules is comparable to the tuning of cells in V1 but the orientation map is less orderly. Horizontal connections in rewired cortex are more patchy and periodic than connections in normal auditory cortex, but less so than connections in V1. These data show that afferent activity has a profound influence on diverse components of cortical circuitry, including thalamocortical and local intracortical connections, which are involved in the generation of orientation tuning, and long-range horizontal connections, which are important in creating an orientation map.

433 citations


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

  • ...They show species specificity (e.g., Van Hooser et al., 2006) and are altered by cross-modal circuit manipulation dur- ing development, reflecting an organization consistent with the new inputs (Gao and Pallas, 1999; Sharma et al., 2000)....

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  • ...ing development, reflecting an organization consistent with the new inputs (Gao and Pallas, 1999; Sharma et al., 2000)....

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