Dynamic organization of primary motor cortex output to target muscles in adult rats II. Rapid reorganization following motor nerve lesions

Donoghue, John P.; Suner, Selim; Sanes, Jerome N.

doi:10.1007/bf00229319

Cited by 299 publications

(140 citation statements)

References 41 publications

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“…In adult macaque monkeys, squirrel monkeys, and prosimian galagos studied years after a therapeutic amputation of a limb after injuries as infants, juveniles, or adults, microstimulation of the territories in M1 of the missing limb evoked movements of the limb stump and adjoining shoulder or trunk at threshold current levels comparable to those for evoked movements in normal primates (15,27,28). Similar results have been obtained in rats (29). Thus, regardless of the age at which the amputation occurs, the deprived portion of motor cortex does not remain nonfunctional but instead mediates new muscle movements.…”

Section: Discussionsupporting

confidence: 69%

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: Discussionsupporting

confidence: 69%

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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“…The areas are adjacent, and so can be easily studied in vitro in the same slice at the same time, yet they are distinct in both lamination and in function. Synaptic modifications demonstrable in vitro may be involved in cortical functions and reorganization in vivo, and both somatosensory and motor areas of the adult rat can reorganize in response to central or peripheral manipulations (Donoghue et al, 1990;Castro-Alamancos et al, 1992;Recanzone et al, 1992;Diamond et al, 1993). Our results show that while motor and somatosensory cortex can express a variety of types of synaptic plasticity, they are not identical in their capabilities.…”

mentioning

confidence: 70%

Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex

1995

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We have studied vertical synaptic pathways in two cytoarchitectonically distinct areas of rat neocortex--the granular primary somatosensory (SI) area and the agranular primary motor (MI) area--and tested their propensity to generate long-term potentiation (LTP), long-term depression (LTD), and related forms of synaptic plasticity. Extracellular and intracellular responses were recorded in layer II/III of slices in vitro while stimulating in middle cortical layers (in or around layer IV). Under control conditions, 5 Hz theta-burst stimulation produced LTP in the granular area, but not in the agranular area. Agranular cortex did generate short-term potentiation that decayed within 20 min. Varying the inter-burst frequency from 2 Hz to 10 Hz reliably yielded LTP of 21–34% above control levels in granular cortex, but no lasting changes were induced in agranular cortex. However, the agranular cortex was capable of generating LTP if a GABAA receptor antagonist was applied locally at the recording site during the induction phase. In contrast to LTP, an identical form of homosynaptic LTD could be induced in both granular and agranular areas by applying low frequency stimulation (1 Hz for 15 min) to the middle layers. Under control conditions, both LTP and LTD were synapse- specific; theta-burst or low-frequency stimulation in the vertical pathway did not induce changes in responses to stimulation of a layer II/III horizontal pathway. Application of the NMDA receptor antagonist D-2-amino-5-phosphonovaleric acid (AP5) blocked the induction of both LTP and LTD in granular and agranular cortex. In the presence of AP5, low-frequency conditioning stimuli yielded a short-term depression in both areas that decayed within 10–15 min. Nifedipine, which blocks L- type, voltage-sensitive calcium channels, slightly depressed the magnitudes of LTP and LTD but did not abolish them. Synaptic responses evoked during theta-burst stimulation were strikingly different in granular and agranular areas. Responses in granular cortex were progressively facilitated during each sequence of 10 theta-bursts, and from sequence-to-sequence; in contrast, responses in agranular cortex were stable during an entire theta-burst tetanus. The results suggest that vertical pathways in primary somatosensory cortex and primary motor cortex express several forms of synaptic plasticity. They were equally capable of generating LTD, but the pathways in somatosensory cortex much more reliably generated LTP, unless inhibition was reduced. LTP may be more easily produced in sensory cortex because of the pronounced synaptic facilitation that occurs there during repetitive stimulation of the induction phase.

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“…The total areal extent of individual forelimb and vibrissa representations was determined with image analysis software (N IH Image, version 1.61) by analyzing identically scaled images of each map. Only the areal extents of the vibrissa and forelimb representations were determined, because: (1) it was expected that vibrissa trimming could affect the size of the vibrissa representation; (2) the forelimb representation shares the longest, common border with the vibrissa representation in comparison with any other neighboring M1 representation; and (3) there is previous evidence that the position of the forelimb -vibrissa border can change under a variety of peripheral manipulations (e.g., Donoghue et al, 1990;Sanes et al, 1992), thus leading to the possibility of reciprocal changes in size of both representations. For each group, the resulting sizes of individual forelimb and vibrissa representations for each animal comprising that group were used for two types of analysis: (1) within-group comparisons between the left experimental hemisphere (defined as M1 contralateral to the trimmed vibrissae) and the right hemisphere (defined as M1 ipsilateral to the trimmed vibrissae), in which statistically significant differences in mean size were determined using paired Student's t tests (level of significance, p Ͻ 0.05); and (2) across-group comparisons between left experimental hemispheres or right hemispheres, in which statistically significant differences were determined using one-way ANOVA and a Scheffé's post hoc test (level of significance, p Ͻ 0.05).…”

Section: Methodsmentioning

confidence: 99%

Differential Effects of Abnormal Tactile Experience on Shaping Representation Patterns in Developing and Adult Motor Cortex

Huntley

1997

J. Neurosci.

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This study investigates the influence of early somatosensory experience on shaping movement representation patterns in motor cortex. Electrical microstimulation was used to map bilaterally the motor cortices of adult rats subjected to altered tactile experience by unilateral vibrissa trimming from birth (birth-trimmed group) or for comparable periods that began in adulthood (adult-trimmed group). Findings demonstrated that (1) vibrissa trimming from birth, but not when initiated in adulthood, led to a significantly smaller-sized primary motor cortex (M1) vibrissa representation in the hemisphere contralateral to the trimmed vibrissae, with no evidence for concomitant changes in size of the adjacent forelimb representation or the representation of the intact vibrissae in the opposite (ipsilateral) hemisphere; (2) in the contralateral hemispheres of the birthtrimmed group, an abnormal pattern of evoked vibrissa movement was evident in which bilateral or ipsilateral (intact) vibrissa movement predominated; (3) in both hemispheres of the birthtrimmed group, current thresholds for eliciting movement of the trimmed vibrissa were significantly lower than normal; and (4) in the adult-trimmed group, but not in the birth-trimmed group, there was a decrease bilaterally in the relative frequency of dual forelimb-vibrissa sites that form the common border between these representations. These results show that sensory experience early in life exerts a significant influence in sculpting motor representation patterns in M1. The mature motor cortex is more resistant to the type and magnitude of influence that tactile experience has on developing M1, which may indicate that such an influence is constrained by a developmentally regulated critical period.

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Dynamic organization of primary motor cortex output to target muscles in adult rats II. Rapid reorganization following motor nerve lesions

Cited by 299 publications

References 41 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

Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex

Differential Effects of Abnormal Tactile Experience on Shaping Representation Patterns in Developing and Adult Motor Cortex

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