Intracortical and Thalamocortical Connections of the Hand and Face Representations in Somatosensory Area 3b of Macaque Monkeys and Effects of Chronic Spinal Cord Injuries.
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.
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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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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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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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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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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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01 Jan 1995
TL;DR: For instance, this paper found that lesion-induced brainstem reorganization may be suppressed at either thethalamic orcortical level or at the thalamic level by invasion of the cuneate nucleus by sciatic nerve primary afferents.
Abstract: andneuroanatomical methods wereusedtodetermine theextent towhichneonatal forelimb removal altered theorganization ofthecuneate nucleus andrepresentations ofthefore- andhindlimbs inthe primary somatosensory cortex ofadult rats. Neonatal forelimbremoval resulted ininvasion ofthecuneate nucleus by sciatic nerveprimary afferents anddevelopment ofcuneothalamicprojection neurons withsplit receptive fields that included boththehindlimb andforelimb stump. Mapping in theprimary somatosensory cortex oftheneonatally manipulated adult rats demonstrated abnormalities, butthemajor change observed inthecuneate nucleus wasdemonstrable at only afew(5%) cortical recording sites intheremaining stump representation andthere werenoneatallinthehindlimb representation. Theseresults suggest thatlesion-induced brainstem reorganization maybefunctionally suppressed at either thethalamic orcortical level. Understanding themechanisms that underlie central nervous system reorganization following peripheral nervedamage remains amajor goal ofneurobiology (see refs. 1and2for recent reviews). Functional reorganization following peripheral nervedamage ininfancy oradulthood, whilequite variable, hasbeenwelldocumented inthesomatosensory cortex (1, 2). Similarly, evidence forfunctional reorganization at subcortical somatosensory stations hasbeenreported (3-8). However, relatively fewstudies haveexamined theconsequences ofperipheral nervedamage atmorethanonelevel of theneural axis. Suchanapproach isanecessity ifwearetofully define boththerange ofchanges thatoccurinthecentral nervous system andtherelation between alterations atdifferentlevels oftheneural axis. We haveexamined theconsequences ofneonatal forelimb removal inboththebrainstem andtheneocortex oftheadult ratinordertocompare andcontrast theresults ofthis manipulation atthetwolevels. We chosetoexamine the brainstem because this isthefirst synapse intheascending somatic lemniscal system andthefirst place whereafferents arising fromtwodifferent peripheral locations (forelimb and hindlimb) terminate inclose proximity, inthenuclei cuneatus (Cu) andgracilis (Gr), respectively. We choseprimary somatosensory cortex because ofthewell-studied andreadily assessable mapoftheentire body surface thatcharacterizes this structure.
37 citations
TL;DR: A regular pattern of intrinsic connectivity within V5/MT is suggested, which is consistent with connectivity between sites with a common preference for both direction of motion and binocular depth, and can potentially account for the large suppressive surrounds of V 5/MT neurons.
Abstract: Visual area V5/MT in the rhesus macaque has a distinct functional organization, where neurons with specific preferences for direction of motion and binocular disparity are co-organized in columns or clusters. Here, we analyze the pattern of intrinsic connectivity within cortical area V5/MT in both parasagittal sections of the intact brain and tangential sections from flatmounted cortex using small injections of the retrograde tracer cholera toxin subunit b. Labeled cells were predominantly found in cortical layers 2, 3, and 6. Going along the cortical layers, labeled cells were concentrated in regularly spaced clusters. The clusters nearest to the injection site were approximately 2 mm from its center. In flatmounted cortex, along the dorsoventral axis of V5/MT, we identified further clusters of labeled cells up to 10 mm from the injection site. Quantitative analysis of parasagittal sections estimated average cluster spacing at 2.2 mm; in cortical flatmounts, spacing was 2.3 mm measured radially from the injection site. The results suggest a regular pattern of intrinsic connectivity within V5/MT, which is consistent with connectivity between sites with a common preference for both direction of motion and binocular depth. The long-range connections can potentially account for the large suppressive surrounds of V5/MT neurons.
31 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)....
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TL;DR: None of the authors' injections, including those into the representation of the tongue, labeled neurons in VPMpc, the thalamic taste nucleus, Thus, area 3b does not appear to be involved in processing taste information from theThalamus.
Abstract: Representations of the parts of the oral cavity and face in somatosensory area 3b of macaque monkeys were identified with microelectrode recordings and injected with different neuroanatomical tracers to reveal patterns of thalamic projections to tongue, teeth, and other representations in primary somatosensory cortex. The locations of injection sites and resulting labeled neurons were further determined by relating sections processed to reveal tracers to those processed for myeloarchitecture in the cortex and multiple architectural stains in the thalamus. The ventroposterior medial sub-nucleus (VPM) for touch was identified as separate from the ventroposterior medial parvicellular nucleus (VPMpc) for taste by differential expression of several types of proteins. Our results revealed somatotopically matched projections from VPM to the part of 3b representing intra-oral structures and the face. Retrogradely labeled cells resulting from injections in area 3b were also found in other thalamic nuclei including: anterior pulvinar (Pa), ventroposterior inferior (VPI), ventroposterior superior (VPS), ventroposterior lateral (VPL), ventral lateral (VL), centre median (CM), central lateral (CL), and medial dorsal (MD). None of our injections, including those into the representation of the tongue, labeled neurons in VPMpc, the thalamic taste nucleus. Thus, area 3b does not appear to be involved in processing taste information from the thalamus. This result stands in contrast to those reported for New World monkeys.
24 citations
"Intracortical and Thalamocortical C..." refers result in this paper
...Normal thalamocortical connections and the somatotopy in the VP nucleus of thalamus have been described by many laboratories, and our data conform to previous reports (Jones and Friedman, 1982; Darian-Smith et al., 1990; Krubitzer and Kaas, 1992; Padberg et al., 2009; Cerkevich et al., 2013)....
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TL;DR: In monkeys with long-term unilateral lesions of the dorsal columns at cervical levels, tactile stimulation of the chin showed BOLD activation in the deafferented hand region of contralesional area 3b in the post-central gyrus.
Abstract: Somatosensory cortex of adult primates undergoes topographic reorganization following spinal cord or peripheral nerve injuries. Electrophysiological studies in monkeys show that after chronic lesions of dorsal columns of the spinal cord at cervical levels, there is an expansion of face representation into the deafferented hand region of area 3b of cortex. However, these techniques can sample only a limited portion of the brain. In order to help understand mechanisms of brain reorganization use of noninvasive tools in non-human primate experimental model is important. Use of blood oxygen level dependent-functional magnetic resonance imaging (BOLD-fMRI) to study brain reorganization in non-human primates has been extremely limited. Here, we show that in monkeys with long-term unilateral lesions of the dorsal columns at cervical levels, tactile stimulation of the chin showed BOLD activation in the deafferented hand region of contralesional area 3b in the post-central gyrus. In a monkey with a partial lesion of the dorsal columns, stimulations of both hand and chin activated the partially deafferented hand region. We also show that the somatotopic organization in the non-deafferented ipsilesional somatosensory cortex remained normal.
18 citations
"Intracortical and Thalamocortical C..." refers background in this paper
...All monkeys were part of other related experiments (Dutta et al., 2014; Kambi et al., 2014, and other unpublished studies)....
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TL;DR: The results suggest that rats have a second rostrally located motor area with RWA and RFA as its constituents.
Abstract: In primates, the motor cortex consists of at least seven different areas, which are involved in movement planning, coordination, initiation, and execution. However, for rats, only the primary motor cortex has been well described. A rostrally located second motor area has been proposed, but its extent, organization, and even definitive existence remain uncertain. Only a rostral forelimb area (RFA) has been definitively described, besides few reports of a rostral hindlimb area. We have previously proposed existence of a second whisker area, which we termed the rostral whisker area (RWA), based on its differential response to intracortical microstimulation compared with the caudal whisker area (CWA) in animals under deep anesthesia (Tandon et al. [2008] Eur J Neurosci 27:228). To establish that RWA is distinct from the caudally contiguous CWA, we determined sources of thalamic inputs to the two proposed whisker areas. Sources of inputs to RFA, caudal forelimb area (CFA), and caudal hindlimb region were determined for comparison. The results show that RWA and CWA can be distinguished based on differences in their thalamic inputs. RWA receives major projections from mediodorsal and ventromedial nuclei, whereas the major projections to CWA are from the ventral anterior, ventrolateral, and posterior nuclei. Moreover, the thalamic nuclei that provide major inputs to RWA are the same as for RFA, and the nuclei projecting to CWA are same as for CFA. The results suggest that rats have a second rostrally located motor area with RWA and RFA as its constituents.
14 citations
"Intracortical and Thalamocortical C..." refers methods in this paper
...In addition, we analyzed parasagittal brain sections from three monkeys that were available in the laboratory from other experiments, and stained for Nissl substance, AChE, or CO to determine distance of area 3b borders from the lip and the fundus of the central sulcus....
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...Locations of the labeled neurons were plotted using Neurolucida software (Microbrightfield) coupled to a computercontrolled microscopic stage with direct visualization through the eye piece as described previously (Mohammed and Jain, 2014)....
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...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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