Deactivation and reactivation of somatosensory cortex after dorsal spinal cord injury

Jain, Neeraj; Catania, Kenneth C.; Kaas, Jon H.

doi:10.1038/386495a0

Cited by 194 publications

(230 citation statements)

References 24 publications

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“…The lesions at cervical levels (C3-4 or C5) sectioned all or most ascending somatosensory afferents from the forelimb, and afferents from the lower body (3,(10)(11)(12). As expected, few neurons in contralateral somatosensory cortex (area 3b) were activated by tactile stimulation of the hand, and the somatotopy was grossly abnormal, as reported previously by Jain et al (7,13,14). Microstimulation results from M1 were obtained by stimulating in long microelectrode penetrations down the cortex of the anterior bank of the central sulcus, or from M1 on the brain surface at depths of ∼1.8 mm (Fig.…”

Section: Resultssupporting

confidence: 57%

Functional organization of motor cortex of adult macaque monkeys is altered by sensory loss in infancy

Jain

Collins

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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When somatosensory cortex (S1) is deprived of some of its inputs after section of ascending afferents in the dorsal columns of the spinal cord, it reorganizes to overrepresent the surviving inputs. As somatosensory cortex provides guiding sensory information to motor cortex, such sensory loss and representational reorganization could affect the development of the motor map in primary motor cortex (M1), especially if the sensory loss occurs early in development. To address this possibility, the dorsal columns of the spinal cord were sectioned between cervical levels (C3-5) 3-12 days after birth in five macaque monkeys. After 3-5 years of maturation (young adults), we determined how movements were represented in M1 contralateral to the lesion by using microelectrodes to electrically stimulate sites in M1 to evoke movements. Although the details of the motor maps in these five monkeys varied, the forelimb motor maps were abnormal. The representations of digit movements were reduced and abnormally arranged. Current levels for evoking movements from the forelimb region of M1 were in the normal range, but the lowest mean stimulation thresholds were for wrist or elbow instead of digit movements. Incomplete lesions and bilateral lesions produced fewer abnormalities. The results suggest that the development of normal motor cortex maps in M1 depends on sensory feedback from somatosensory maps.intracortical microstimulation | motor map | primate | sensory deprivation | spinal cord injury S ensory guidance plays an important role in movement control.When the somatosensory afferents from the forearm are removed or reduced in number by section of the dorsal roots or dorsal columns, monkeys become reluctant to use the affected forelimb, although they can be trained to do so (1-3). This reluctance to use the affected limb can largely be attributed to sensory loss. However, when the sensory loss is incomplete, the somatosensory system reorganizes over time so that cortical neurons deprived of their normal sources of activation become responsive to preserved somatosensory inputs (3-7). Most notably, a partial loss of inputs from the hand is followed by the reactivation of deprived parts of somatosensory cortex (area 3b) by preserved inputs from the hand, and even inputs from the face over longer periods of recovery. This reactivation produces a distorted sensory map in area 3b that no longer represents some parts of the hand and overrepresents others. This distorted map relays less than optimal sensory information to higher order sensory representations (8) and then to motor cortex, possibly altering the somatotopy of the motor representation in developing or even mature monkeys. Postlesion changes in the cortical motor map could reflect an altered use of the hand after the sensory loss, as motor cortex organization is shaped by experience (9).Here we used electrical microstimulation techniques to study the organization of primary motor cortex of young adult macaque monkeys reared from infancy with a sensory loss produced by a le...

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Section: Resultssupporting

confidence: 57%

Functional organization of motor cortex of adult macaque monkeys is altered by sensory loss in infancy

Jain

Collins

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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“…Data from other laboratories show, for example, that sprouting of spared primary afferents did not occur within the rat gracile nuclei between 5 days and 3 months after incomplete thoracic spinal cord dorsal column injury (Jain et al, 1995) nor within the non-human primate cuneate nuclei 5 days after incomplete cervical spinal cord dorsal column injury (Jain et al, 1997). Conditioning sciatic nerve injury to increase regenerative capacity (Richardson and Issa, 1984) failed to promote sprouting of spared primary afferents in the rat gracile nuclei during the first week after contusive thoracic SCI (Baker and Hagg, 2005).…”

Section: Discussionmentioning

confidence: 96%

Loss and spontaneous recovery of forelimb evoked potentials in both the adult rat cuneate nucleus and somatosensory cortex following contusive cervical spinal cord injury

Onifer

Nunn

Decker

et al. 2007

Experimental Neurology

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Varying degrees of neurologic function spontaneously recovers in humans and animals during the days and months after spinal cord injury (SCI). For example, abolished upper limb somatosensory potentials (SSEPS) and cutaneous sensations can recover in persons post-contusive cervical SCI. To maximize recovery and the development/evaluation of repair strategies, a better understanding of the anatomical locations and physiological processes underlying spontaneous recovery after SCI is needed. As an initial step, the present study examined whether recovery of upper limb SSEPs after contusive cervical SCI was due to the integrity of some spared dorsal column primary afferents that terminate within the cuneate nucleus and not one of several alternate routes. C5-C6 contusions were performed on male adult rats. Electrophysiological techniques were used in the same rat to determine forelimb evoked neuronal responses in both cortex (SSEPS) and the cuneate nucleus (terminal extracellular recordings). SSEPs were not evoked 2 days post-SCI but were found at 7 days and beyond, with an observed change in latencies between 7 and 14 days (suggestive of spared axon remyelination). Forelimb evoked activity in the cuneate nucleus at 15 but not 3 days post-injury occurred despite dorsal column damage throughout the cervical injury (as seen histologically). Neuroanatomical tracing (using 1% unconjugated cholera toxin B subunit) confirmed that upper limb primary afferent terminals remained within the cuneate nuclei. Taken together, these results indicate Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. NIH Public Access

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“…Moreover, recovery of hindlimb placing was associated with axon sprouting. Additionally, Jain et al [27] observed that complete lesions of the primate cervical spinal cord dorsal columns deactivated the forelimb, trunk, and hind limb representations in the somatosensory cortex. Afferents from the face reactivated these deactivated representations.…”

Section: Spontaneous Functional Return and Recovery After Scimentioning

confidence: 99%

“…Associated with this was sprouting of trigeminal primary afferents into the brainstem cuneate nuclei, the target of forelimb and other upper extremity primary afferents [28]. Incomplete lesions of the dorsal columns led to sprouting of spared forelimb primary afferents in the cuneate nuclei and reactivation of forelimb representations [24,27]. In contrast, reactivation of hind limb representations in the rat somatosensory cortex did not occur following incomplete lesions of the thoracic spinal cord dorsal columns [29].…”

Section: Spontaneous Functional Return and Recovery After Scimentioning

confidence: 99%

Plasticity After Spinal Cord Injury: Relevance to Recovery and Approaches to Facilitate It

2011

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Summary: Motor, sensory, and autonomic functions can spontaneously return or recover to varying extents in both humans and animals, regardless of the traumatic spinal cord injury (SCI) level and whether it was complete or incomplete. In parallel, adverse and painful functions can appear. The underlying mechanisms for all of these diverse functional changes are summarized under the term plasticity. Our review will describe what is known regarding this phenomenon after traumatic SCI and focus on its relevance to motor and sensory recovery. Although it is still somewhat speculative, plasticity can be found throughout the neuraxis and includes various changes ranging from alterations in the properties of spared neuronal circuitries, intact or lesioned axon collateral sprouting, and synaptic rearrangements. Furthermore, we will discuss a selection of potential approaches for facilitating plasticity as possible SCI treatments. Because a mechanism underlying spontaneous plasticity and recovery might be motor activity and the related neuronal activity, activity-based therapies are being used and investigated both clinically and experimentally. Additional pharmacological and gene-delivery approaches, based on plasticity being dependent on the delicate balance between growth inhibition and promotion as well as the basic intrinsic growth ability of the neurons themselves, have been found to be effective alone and in combination with activitybased therapies. The positive results have to be tempered with the reality that not all plasticity is beneficial. Therefore, a tremendous number of questions still need to be addressed. Ultimately, answers to these questions will enhance plasticity's potential for improving the quality of life for persons with SCI.

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Deactivation and reactivation of somatosensory cortex after dorsal spinal cord injury

Cited by 194 publications

References 24 publications

Functional organization of motor cortex of adult macaque monkeys is altered by sensory loss in infancy

Functional organization of motor cortex of adult macaque monkeys is altered by sensory loss in infancy

Loss and spontaneous recovery of forelimb evoked potentials in both the adult rat cuneate nucleus and somatosensory cortex following contusive cervical spinal cord injury

Plasticity After Spinal Cord Injury: Relevance to Recovery and Approaches to Facilitate It

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