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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 ArticleDOI
TL;DR: Somatotopic maps in the mature brain reorganize in response to deafferentation by peripheral nerve cut, amputations, or spinal lesions, and an understanding of these mechanisms could guide interventions that potentiate recovery from such injuries.
Abstract: Somatotopic maps in the mature brain reorganize in response to deafferentation by peripheral nerve cut, amputations, or spinal lesions. Mechanisms underlying these changes may range from altered tonic inhibition and synaptic efficacy to neuronal sprouting. An understanding of these mechanisms could guide interventions that potentiate recovery from such injuries.

103 citations


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

  • ...The hand–face border, which is easily seen in histological sections as myelin-light septa in different species of monkeys (Jain et al., 1998b; Iyengar et al., 2007), likely forms a limiting boundary for information exchange between regions receiving nonadjacent peripheral inputs from hand and face....

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  • ...In all these cases, the cortex was flattened and a series of alternate sections was stained for myelin to reveal the HFS (Jain et al., 1998b), which confirmed that the injection core did not cross the hand– face border....

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  • ...…of intact chin inputs into the deafferented hand region of primary somatosensory area 3b, second somatosensory area S2, parietal ventral area PV (Jain et al., 1997, 1998a; Kaas et al., 2008; Tandon et al., 2009), ventroposterior (VP) nucleus of Received May 26, 2015; revised Aug. 24, 2015;…...

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  • ...Adjacent sections, stained for myelin, were drawn at the same magnification, and myeloarchitectonic features and HFS were marked (Jain et al., 1998b)....

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  • ...Other series of sections were stained for myelin using a modified Gallyas procedure (Jain et al., 1998b) to visualize the hand–face border in area 3b, which is visible as hand–face septum (HFS) (Fig....

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Journal ArticleDOI
TL;DR: Findings from fMRI at 3T during imagined hand and foot movements are interpreted as evidence that BCI training as a conduit of motor imagery training may assist in maintaining access to SMC in largely preserved somatopy despite complete deafferentation.
Abstract: Although several features of brain motor function appear to be preserved even in chronic complete SCI, previous functional MRI (fMRI) studies have also identified significant derangements such as a strongly reduced volume of activation, a poor modulation of function and abnormal activation patterns. It might be speculated that extensive motor imagery training may serve to prevent such abnormalities. We here report on a unique patient with a complete traumatic SCI below C5 who learned to elicit electroencephalographic signals beta-bursts in the midline region upon imagination of foot movements. This enabled him to use a neuroprosthesis and to "walk from thought" in a virtual environment via a brain-computer interface (BCI). We here used fMRI at 3T during imagined hand and foot movements to investigate the effects of motor imagery via persistent BCI training over 8 years on brain motor function and compared these findings to a group of five untrained healthy age-matched volunteers during executed and imagined movements. We observed robust primary sensorimotor cortex (SMC) activity in expected somatotopy in the tetraplegic patient upon movement imagination while such activation was absent in healthy untrained controls. Sensorimotor network activation with motor imagery in the patient (including SMC contralateral to and the cerebellum ipsilateral to the imagined side of movement as well as supplementary motor areas) was very similar to the pattern observed with actual movement in the controls. We interpret our findings as evidence that BCI training as a conduit of motor imagery training may assist in maintaining access to SMC in largely preserved somatopy despite complete deafferentation.

98 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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Journal ArticleDOI
TL;DR: It is shown that large-scale reorganization in area 3b following spinal cord injuries is due to changes at the level of the brainstem nuclei and not due to cortical mechanisms.
Abstract: Adult mammalian brains undergo reorganization following deafferentations due to peripheral nerve, cortical or spinal cord injuries. The largest extent of cortical reorganization is seen in area 3b of the somatosensory cortex of monkeys with chronic transection of the dorsal roots or dorsal columns of the spinal cord. These injuries cause expansion of intact face inputs into the deafferented hand cortex, resulting in a change of representational boundaries by more than 7 mm. Here we show that large-scale reorganization in area 3b following spinal cord injuries is due to changes at the level of the brainstem nuclei and not due to cortical mechanisms. Selective inactivation of the reorganized cuneate nucleus of the brainstem eliminates observed face expansion in area 3b. Thus, the substrate for the observed expanded face representation in area 3b lies in the cuneate nucleus.

98 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....

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  • ...There was sparing of the medial part of fasciculus cuneatus and nearly complete touch on the chin (Kambi et al., 2014, somatotopic map of their Fig....

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  • ..., 2008), and cuneate nucleus of the brainstem (Kambi et al., 2014)....

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  • ...that drives cortical reorganization (Kambi et al., 2014)....

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  • ...We have recently shown that reorganization of the cuneate nucleus is the critical change that drives cortical reorganization (Kambi et al., 2014)....

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Journal ArticleDOI
TL;DR: Electrophysiological mapping demonstrated the finer details of the representations of the hand, lower jaw, neck, and face in area 3b of normal macaque monkeys, and horizontal intracortical connections may form one substrate for representational plasticity in somatosensory cortex.
Abstract: Horizontal intracortical connections may form one substrate for representational plasticity in somatosensory cortex. Electrophysiological mapping demonstrated the finer details of the representations of the hand, lower jaw, neck, and face in area 3b of normal macaque monkeys. Injections of two fluorescent tracers then defined the extent to which horizontal connections crossed from the face into the hand representations and vice versa in area 3b. Connections are widely distributed within cortical representations of skin areas innervated by cervical nerves or by the trigeminal nerve but do not cross a border defined by the anterior limit of the representation of skin innervated by the second cervical nerve. This border separates the representation of the muzzle, innervated only by the mandibular nerve, and the representation of the lower jaw and neck region, innervated by the second and third cervical nerves but overlapped by the mandibular nerve. Thus, the muzzle representation lacks connections with the hand and with the lower jaw and neck representations, but the representations of the hand and of the lower jaw and neck are strongly interconnected. Overlap of the hand and of the lower jaw and neck representations and of their horizontal intracortical connections may form one basis for expansions of the lower jaw representation into that of the hand when peripheral input from the hand is lost. Lack of connections with the rest of the face representation may limit this spread.

93 citations


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

  • ...The Jones laboratory has examined connectivity across the hand–face border in macaque monkeys (Manger et al., 1997)....

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  • ...Because data from normal macaque monkeys are extremely limited (Manger et al., 1997), we also determined the intrinsic connections in normal monkeys....

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Journal ArticleDOI
TL;DR: It is demonstrated that horizontal and feedback modulation of strong recurrent circuits allows the tuning of contextual effects to change with changing feedforward inputs, and that this tuning behavior is instead highly prevalent in V1.
Abstract: In macaque primary visual cortex (V1), neuronal responses to stimuli inside the receptive field (RF) are modulated by stimuli in the RF surround. This modulation is orientation specific. Previous studies suggested that, for some cells, this specificity may not be fixed but changes with the stimulus orientation presented to the RF. We demonstrate, in recording studies, that this tuning behavior is instead highly prevalent in V1 and, in theoretical work, that it arises only if V1 operates in a regime of strong local recurrence. Strongest surround suppression occurs when the stimuli in the RF and the surround are iso-oriented, and strongest facilitation when the stimuli are cross-oriented. This is the case even when the RF is suboptimally activated by a stimulus of nonpreferred orientation but only if this stimulus can activate the cell when presented alone. This tuning behavior emerges from the interaction of lateral inhibition (via the surround pathways), which is tuned to the preferred orientation of the RF, with weakly tuned, but strong, local recurrent connections, causing maximal withdrawal of recurrent excitation at the feedforward input orientation. Thus, horizontal and feedback modulation of strong recurrent circuits allows the tuning of contextual effects to change with changing feedforward inputs.

92 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)....

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