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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TL;DR: It is concluded that long-range horizontal projections contribute to the dominant input underlying the capacity for retinal lesion-induced plasticity in V1.
Abstract: The placement of monocular laser lesions in the adult cat retina produces a lesion projection zone (LPZ) in primary visual cortex (V1) in which the majority of neurons have a normally located receptive field (RF) for stimulation of the intact eye and an ectopically located RF (displaced to intact retina at the edge of the lesion) for stimulation of the lesioned eye. Animals that had such lesions for 14-85 d were studied under halothane and nitrous oxide anesthesia with conventional neurophysiological recording techniques and stimulation of moving light bars. Previous work suggested that a candidate source of input, which could account for the development of the ectopic RFs, was long-range horizontal connections within V1. The critical contribution of such input was examined by placing a pipette containing the neurotoxin kainic acid at a site in the normal V1 visual representation that overlapped with the ectopic RF recorded at a site within the LPZ. Continuation of well defined responses to stimulation of the intact eye served as a control against direct effects of the kainic acid at the LPZ recording site. In six of seven cases examined, kainic acid deactivation of neurons at the injection site blocked responsiveness to lesioned-eye stimulation at the ectopic RF for the LPZ recording site. We therefore conclude that long-range horizontal projections contribute to the dominant input underlying the capacity for retinal lesion-induced plasticity in V1.
80 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....
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...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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TL;DR: Using intracortical microstimulation (ICMS) it is shown that movements evoked in the whisker and the neck region of the rat motor cortex are highly sensitive to the depth of anaesthesia.
Abstract: The primary motor cortex of mammals has an orderly representation of different body parts Within the representation of each body part the organization is more complex, with groups of neurons representing movements of a muscle or a group of muscles In rats, uncertainties continue to exist regarding organization of the primary motor cortex in the whisker and the neck region Using intracortical microstimulation (ICMS) we show that movements evoked in the whisker and the neck region of the rat motor cortex are highly sensitive to the depth of anaesthesia At light anaesthetic depth, whisker movements are readily evoked from a large medial region of the motor cortex Lateral to this is a small region where movements of the neck are evoked However, in animals under deep anaesthesia whisker movements cannot be evoked Instead, neck movements are evoked from this region The neck movement region thus becomes greatly expanded An analysis of the threshold currents required to evoke movements at different anaesthetic depths reveals that the caudal portion of the whisker region has dual representation, of both the whisker and the neck movements The results also underline the importance of carefully controlling the depth of anaesthesia during ICMS experiments
79 citations
"Intracortical and Thalamocortical C..." refers background in this paper
...Neuronal responses to manual movements of the limb and digits, as well as joint manipulations, were also determined (Tandon et al., 2008)....
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TL;DR: It is found that the somatosensory thalamus is composed of several representations of cutaneous and deep receptors of the contralateral body, which indicate that multiple inputs are processed simultaneously within and across several, "hierarchically connected" cortical fields.
Abstract: We examined the organization and cortical projections of the somatosensory thalamus using multiunit microelectrode recording techniques in anesthetized monkeys combined with neuroanatomical tracings techniques and architectonic analysis Different portions of the hand representation in area 3b were injected with different anatomical tracers in the same animal, or matched body part representations in parietal areas 3a, 3b, 1, 2, and areas 2 and 5 were injected with different anatomical tracers in the same animal to directly compare their thalamocortical connections We found that the somatosensory thalamus is composed of several representations of cutaneous and deep receptors of the contralateral body These nuclei include the ventral posterior nucleus, the ventral posterior superior nucleus, the ventral posterior inferior nucleus, and the ventral lateral nucleus Each nucleus projects to several different cortical fields, and each cortical field receives projections from multiple thalamic nuclei In contrast to other sensory systems, each of these somatosensory cortical fields is uniquely innervated by multiple thalamic nuclei These data indicate that multiple inputs are processed simultaneously within and across several, “hierarchically connected” cortical fields
74 citations
"Intracortical and Thalamocortical C..." refers background or result in this paper
...These locations correspond to representations of D1 and chin in the VP nucleus (Jones and Friedman, 1982; Kaas et al., 1984; Darian-Smith et al., 1990; Burton and Fabri, 1995; Padberg et al., 2009)....
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...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: It is stressed that the understanding of the neuroplastic changes that occur in sensory-deprived individuals may help guide the design and the implementation of such rehabilitative methods, and two promising rehabilitative strategies based on opposing theoretical principles will be considered.
Abstract: The purpose of this review is to consider new sensory rehabilitation avenues in the context of the brain's remarkable ability to reorganize itself following sensory deprivation. Here, deafness and blindness are taken as two illustrative models. Mainly, two promising rehabilitative strategies based on opposing theoretical principles will be considered: sensory substitution and neuroprostheses. Sensory substitution makes use of the remaining intact senses to provide blind or deaf individuals with coded information of the lost sensory system. This technique thus benefits from added neural resources in the processing of the remaining senses resulting from crossmodal plasticity, which is thought to be coupled with behavioral enhancements in the intact senses. On the other hand, neuroprostheses represent an invasive approach aimed at stimulating the deprived sensory system directly in order to restore, at least partially, its functioning. This technique therefore relies on the neuronal integrity of the brain areas normally dedicated to the deprived sense and is rather hindered by the compensatory reorganization observed in the deprived cortex. Here, we stress that our understanding of the neuroplastic changes that occur in sensory-deprived individuals may help guide the design and the implementation of such rehabilitative methods.
74 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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TL;DR: The study of anatomy of horizontal connections and characterized horizontal functional interactions in V1 of the gray squirrel suggests that periodic and patchy connectivity is not a universal organizing principle of cortex, and the existence of patchy and periodic connectivity and functional maps may be linked.
Abstract: In the cerebral cortex of mammals, horizontal connections link cells up to several millimeters apart. In primary visual cortex (V1) of mammals with orientation maps, horizontal connections ramify in periodic patches across the cortical surface, connecting cells with similar orientation preferences. Rodents have orientation-selective cells but lack orientation maps, raising questions about relationships of horizontal connections to functional maps and receptive field properties. To address these questions, we studied anatomy of horizontal connections and characterized horizontal functional interactions in V1 of the gray squirrel, a highly visual rodent. Long-range intrinsic connections in squirrel V1 extended 1-2 mm but were not patchy or periodic. This result suggests that periodic and patchy connectivity is not a universal organizing principle of cortex, and the existence of patchy and periodic connectivity and functional maps may be linked. In multielectrode and intracellular recordings, we found evidence of unselective local interactions among cells, similar to pinwheel centers of carnivores. These data suggest that, in mammals with and without orientation maps, local connections link near neighbors without regard to orientation selectivity. In single-unit recordings, we found length-summing and end-stopped cells that were similar to those in other mammals. Length-summing cell surrounds were orientation selective, whereas surrounds of end-stopped cells were not. Receptive field response classes are quite similar across mammals, and therefore patchy and columnar connectivity may not be essential for these properties.
71 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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