scispace - formally typeset
Search or ask a question
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
More filters
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]....

    [...]

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)....

    [...]

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)....

    [...]

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)....

    [...]

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
More filters
Journal ArticleDOI
TL;DR: The findings suggest that novel innocuous somatosensory experiences produce changes in the receptive field configuration of cortical cells that are consistent with Hebbian theories of experience-dependent potentiation and weakening of synaptic efficacy within SI neocortical circuitry, for correlated and uncorrelated sensory inputs, respectively.
Abstract: The effect of innocuously biasing the flow of sensory activity from the whiskers for periods of 3-30 d in awake, behaving adult rats on the receptive field organization of rat SI barrel cortex neurons was studied One pair of adjacent whiskers, D2 and either D1 or D3, remained intact unilaterally (whisker pairing), all others being trimmed throughout the period of altered sensation Receptive fields of single cells in the contralateral D2 barrel were analyzed under urethane anesthesia by peristimulus time histogram (PSTH) and latency histogram analysis after 3, 7-10, and 30 d of pairing and compared with controls, testing all whiskers cut to the same length Response magnitudes to surround receptive field in-row whiskers D1 and D3 were not significantly different for control animals The same was found for surround in-arc whiskers C2 and E2 However, after 3 d of whisker pairing a profound bias occurred in response to the paired D-row surround whisker relative to the opposite trimmed surround D-row whisker and to the C2 and E2 whiskers This bias increased with the duration of pairing, regardless of which surround whisker (D1 or D3) was paired with D2 For all three periods of pairing the mean response to the paired surround whisker was increased relative to controls, but peaked at 7-10 d Response to the principal center-receptive (D2) whisker was increased for the 3 and 7-10 d groups and then decreased at 30 d Responses to trimmed arc surround whiskers (C2 and E2) were decreased in proportion to the duration of changed experience Analysis of PSTH data showed that earliest discharges (5-10 msec poststimulus) to the D2 whisker increased progressively in magnitude with duration of pairing For the paired surround whisker similar early discharges newly appeared after 30 d of pairing At 3 and 7-10 d of pairing, increases in response to paired whiskers and decreases to cut surround whiskers were confined to late portions of the PSTH (10-100 msec poststimulus) Changes at 3-10 d can be attributed to alterations in intracortical synaptic relay between barrels Longer-term changes in response to both paired whisker inputs (30 d) largely appear to reflect increases in thalamocortical synaptic efficacy Our findings suggest that novel innocuous somatosensory experiences produce changes in the receptive field configuration of cortical cells that are consistent with Hebbian theories of experience-dependent potentiation and weakening of synaptic efficacy within SI neocortical circuitry, for correlated and uncorrelated sensory inputs, respectively

168 citations


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

  • ...In rat whisker barrel cortex, whisker pairing plasticity is more robust across rows compared with across arcs (Armstrong-James et al., 1994), which corresponds with richer intrinsic connections across rows than arcs (Hoeflinger et al....

    [...]

  • ...In rat whisker barrel cortex, whisker pairing plasticity is more robust across rows compared with across arcs (Armstrong-James et al., 1994), which corresponds with richer intrinsic connections across rows than arcs (Hoeflinger et al., 1995)....

    [...]

Journal ArticleDOI
TL;DR: This finding demonstrates a dramatic 'top-down' influence of cortex on receptive field size in the somatosensory thalamus and indicates that changes in 'higher-order' areas of the brain can trigger extensive changes in the receptive field characteristics of neurons located earlier in the processing pathway.
Abstract: The influence of cortical feedback on receptive field organization in the thalamus was assessed in the primate somatosensory system. Chronic and acute suppression of neuronal activity in primary somatosensory cortex resulted in a striking enlargement of receptive fields in the ventroposterior thalamus. This finding demonstrates a dramatic 'top-down' influence of cortex on receptive field size in the somatosensory thalamus. In addition, this result has important implications for studies of adult neuronal plasticity because it indicates that changes in 'higher-order' areas of the brain can trigger extensive changes in the receptive field characteristics of neurons located earlier in the processing pathway.

165 citations


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

  • ...Such sprouting, if present, may not be expressed physiologically (Lane et al., 1995) but could play a role in shaping the novel receptive fields of neurons resulting from reorganizational changes at the medullary level (Faggin et al., 1997; Ergenzinger et al., 1998)....

    [...]

Journal ArticleDOI
TL;DR: The results suggest that the extent of short-term, functional reorganization of M1 induced within the first several hours following peripheral nerve cut is mediated, and constrained, by an anatomical framework of pre-existing, horizontal projections which traverse representation borders.
Abstract: Plasticity of representational maps in adult cerebral cortex has been documented in both sensory and motor cortex, but the anatomical basis for cortical plasticity remains poorly understood. To investigate horizontal connectivity in primary motor cortex (M1) as a putative anatomical substrate for short-term, functional plasticity of adult motor cortical representations, a combination of electrical stimulation and biocytin labeling was used to examine pre-existing patterns of intrinsic connections in adult rat M1 in relationship to the pattern of reorganization of the motor movement map induced by transection of the contralateral facial nerve. Two hours after nerve cut, small, circumscribed regions of the forelimb representation expanded medially into territory previously devoted to the vibrissae representation. Outside of this novel, expanded forelimb region, no forelimb movement could be evoked from the former vibrissae representation at any time over the period of hours tested, thus representing silent cortex. Injections placed into vibrissae cortex representing the newly expanded forelimb representation gave rise to labeled axons and dense terminal fiber labeling which crossed the forelimb/vibrissae border and extended up to 1.2 mm within the low-threshold forelimb representation. In contrast, injections placed into silent vibrissae cortex gave rise to labeled axons and terminal boutons which remained mostly restricted to the original vibrissae representation, with only sparse projections that crossed into the low-threshold forelimb representation. Thus, these results suggest that the extent of short-term, functional reorganization of M1 induced within the first several hours following peripheral nerve cut is mediated, and constrained, by an anatomical framework of pre-existing, horizontal projections which traverse representation borders.

163 citations


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

  • ...Similarly, intrinsic connections play a role in plasticity in the motor cortex and visual cortex (Huntley, 1997; Calford et al., 2003) and help in shaping of isoorientation tuned neuronal responses in V1 (Shushruth et al., 2012)....

    [...]

Journal ArticleDOI
TL;DR: In this paper, the authors used retrograde anatomic tracing and topographic physiologic mapping of acoustic response properties to reveal long-range (≥ 1.5 mm) convergent intrinsic horizontal connections between primary auditory cortex subregions with similar bandwidth and characteristic frequency selectivity.
Abstract: Many response properties in primary auditory cortex (AI) are segregated spatially and organized topographically as those in primary visual cortex. Intensive study has not revealed an intrinsic, anatomical organizing principle related to an AI functional topography. We used retrograde anatomic tracing and topographic physiologic mapping of acoustic response properties to reveal long-range (≥1.5 mm) convergent intrinsic horizontal connections between AI subregions with similar bandwidth and characteristic frequency selectivity. This suggests a modular organization for processing spectral bandwidth in AI.

153 citations


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

  • ...Intrinsic connections restricted to functional compartments have been observed in other systems, including visual, auditory, and motor cortex (Huntley and Jones, 1991; Yoshioka et al., 1996; Read et al., 2001; Ahmed et al., 2012)....

    [...]

Journal ArticleDOI
TL;DR: A comparison of the extents of deafferentation across the monkeys shows that even if the dorsal column lesion is partial, preserving most of the hand representation, it is sufficient to induce an expansion of the face representation.
Abstract: Adult brains undergo large-scale plastic changes after peripheral and central injuries. Although it has been shown that both the cortical and thalamic representations can reorganize, uncertainties exist regarding the extent, nature, and time course of changes at each level. We have determined how cortical representations in the somatosensory area 3b and the ventroposterior (VP) nucleus of thalamus are affected by long standing unilateral dorsal column lesions at cervical levels in macaque monkeys. In monkeys with recovery periods of 22-23 months, the intact face inputs expanded into the deafferented hand region of area 3b after complete or partial lesions of the dorsal columns. The expansion of the face region could extend all the way medially into the leg and foot representations. In the same monkeys, similar expansions of the face representation take place in the VP nucleus of the thalamus, indicating that both these processing levels undergo similar reorganizations. The receptive fields of the expanded representations were similar in somatosensory cortex and thalamus. In two monkeys, we determined the extent of the brain reorganization immediately after dorsal column lesions. In these monkeys, the deafferented regions of area 3b and the VP nucleus became unresponsive to the peripheral touch immediately after the lesion. No reorganization was seen in the cortex or the VP nucleus. A comparison of the extents of deafferentation across the monkeys shows that even if the dorsal column lesion is partial, preserving most of the hand representation, it is sufficient to induce an expansion of the face representation.

152 citations


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

  • ...In normal monkeys, thalamocortical connections were plotted following injections of BDA in D1 representation in Monkeys 09-51NM and 10-31NM, FR in D1 representation in Monkey 11-22NM, and FR in chin representation in Monkey 09-51NM. Plots of retrogradely labeled neurons in VP nucleus of monkeys with injection of neuroanatomical tracer in D1 showed that neurons were confined to the medial-most region of the hand subnucleus of ventral posterior lateral nucleus (VPL), along the lamina between the VPL and VPM (Fig....

    [...]

  • ...However, location of the hand–face border, which is near tip of the intraparietal sulcus, was easy to determine, even in monkeys with lesions, because eliciting neuronal responses to chin stimulation in the deafferented hand region required taps instead of light touch (Jain et al., 2008)....

    [...]

  • ...In the two remaining monkeys (LM105 and LM95), the cortex was not flattened be- cause they were also part of other experiments; therefore, position of the hand–face border was placed near the tip of the intraparietal sulcus (Jain et al., 2008) and estimated from the somatotopic map....

    [...]

  • ...The animals were given antibiotics (enrofloxacin; 5 mg/kg, i.m.), analgesics (diclofenac 1.6 mg/kg, i.m.), and dexamethasone (in reducing dosages starting with 2 mg/kg, i.m.) for 5 d after surgery (Jain et al., 2008)....

    [...]

  • ...…boundaries in the cortex after large deafferentations, 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,…...

    [...]