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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: Recent approaches to characterize meso-scale maps, layer units, and cortical fields in the sensorimotor cortex of the living human brain are reviewed and their impact on theories of perception, motor control, topographic encoding, and cortex plasticity is discussed.

17 citations

Journal ArticleDOI
19 Oct 2021-eLife
TL;DR: In this paper, the authors used functional MRI and a (attempted) finger movement task in tetraplegic patients to characterise the somatotopic hand layout in primary somatosensory cortex.
Abstract: Previous studies showed reorganised and/or altered activity in the primary sensorimotor cortex after a spinal cord injury (SCI), suggested to reflect abnormal processing. However, little is known about whether somatotopically specific representations can be activated despite reduced or absent afferent hand inputs. In this observational study, we used functional MRI and a (attempted) finger movement task in tetraplegic patients to characterise the somatotopic hand layout in primary somatosensory cortex. We further used structural MRI to assess spared spinal tissue bridges. We found that somatotopic hand representations can be activated through attempted finger movements in the absence of sensory and motor hand functioning, and no spared spinal tissue bridges. Such preserved hand somatotopy could be exploited by rehabilitation approaches that aim to establish new hand-brain functional connections after SCI (e.g. neuroprosthetics). However, over years since SCI the hand representation somatotopy deteriorated, suggesting that somatotopic hand representations are more easily targeted within the first years after SCI.

15 citations

Journal ArticleDOI
TL;DR: How the findings from plasticity studies in nonhuman primate models may affect therapeutic interventions for conditions involving sensory loss due to spinal cord injury is suggested.
Abstract: Here, we review recent work on plasticity and recovery after dorsal column spinal cord injury in nonhuman primates. Plasticity in the adult central nervous system has been established and studied for the past several decades; however, capacities and limits of plasticity are still under investigation. Studies of plasticity include assessing multiple measures before and after injury in animal models. Such studies are particularly important for improving recovery after injury in patients. In summarizing work by our research team and others, we suggest how the findings from plasticity studies in nonhuman primate models may affect therapeutic interventions for conditions involving sensory loss due to spinal cord injury.

14 citations

Journal ArticleDOI
01 Aug 2019-Cortex
TL;DR: In this article, the authors report on a patient with brachial plexus avulsion who underwent sensory testing and was asked to report the location of the stimulated site and any other sensations experienced.

13 citations

Posted ContentDOI
09 Feb 2021-bioRxiv
TL;DR: In this article, the authors used functional MRI and an attempted finger movement task to characterise the somatotopic hand layout in the primary somatosensory cortex and structural MRI to assess spared spinal tissue bridges.
Abstract: Following spinal cord injury (SCI), the motor output flow to the limb(s) and sensory input to the brain is largely lost. While attempted movements with the paralysed and sensory deprived body part can still evoke signals in the sensorimotor system, this task-related 9net9 brain activity of SCI patients differs substantially from healthy controls. Such reorganised and/or altered activity is thought to reflect abnormal processing. It is however possible that this altered net sensorimotor activity in SCI patients conceals preserved somatotopically-specific representations of the paralysed and sensory deprived body parts that could be exploited in a functionally meaningful manner (e.g. via neuroprosthetics). In this cross-sectional study, we investigated whether a functional connection between the periphery and the brain is necessary to maintain somatosensory representations. We used functional MRI and an (attempted) finger movement task to characterise the somatotopic hand layout in the primary somatosensory cortex and structural MRI to assess spared spinal tissue bridges. We tested 14 tetraplegic SCI patients (mean age, s.e.m.=55, 3.6; 1 female) who differed in terms of lesion completeness, retained sensorimotor functioning, and time since injury, as well as 18 healthy control participants (mean age, s.e.m.=56, 3.6 years; 1 female). Our results revealed somatotopically organised representations of patients9 hands in which neighbouring clusters showed selectivity for neighbouring fingers in contralateral S1, qualitatively similar to those observed in healthy controls. To quantify whether these representations were normal in tetraplegic SCI patients we correlated each participant9s intricate representational distance pattern across all fingers (revealed using representational similarity analysis) with a canonical inter-finger distance pattern obtained from an independent sample. The resulting hand representation typicality scores were not significantly different between patients and controls. This was even true when considering two individual patients with no sensory hand functioning, no hand motor functioning, and no spared spinal tissue bridges. However, a correlational analysis revealed that over years since SCI the hand representation typicality in primary somatosensory cortex deteriorates. We show that somatosensory representations can be maintained for several years following SCI even in the absence of perhiperhal inputs. Such preserved cortical hand representations could therefore be exploited in a functionally meaningful way by rehabilitation approaches that attempt to establish new functional connections between the hand and the brain after an SCI (e.g. through neuroprosthetics). However, time since injury may critically influence the somatotopic representations of SCI patients and might thereby impact the success of such rehabilitation approaches.

11 citations

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.,…...

    [...]

  • ...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)....

    [...]

  • ...…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)....

    [...]

  • ...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)....

    [...]

  • ...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)....

    [...]

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)....

    [...]

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

    [...]

  • ...…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)....

    [...]

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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