The Reorganization of Somatosensory Cortex Following Peripheral Nerve Damage in Adult and Developing Mammals

Kaas, J.H.; Merzenich, M. M.; Killackey, Herbert P.

doi:10.1146/annurev.ne.06.030183.001545

Cited by 611 publications

(261 citation statements)

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“…On the other hand, as reflected by abnormally large proportions of neurons that were unresponsive to cutaneous stimuli, or by unresponsive cortical zones, there is also some agreement that nerve transection results in a loss of cutaneous responsiveness in cortex (Table 2, studies A, C, and D, column 7). These cortical reactions are generally consistent with findings from a larger body of studies dealing with cortical (for a recent review, see Kaas et al, 1983) and subcortical a Other early studies indicated that experiments had been done on young and adult animals but no results were presented for adult animals and age-related differences were not discussed (Pidoux et al, 1979(Pidoux et al, , 1980Waite and Taylor, 1978). Vol.…”

Section: Present Jindingssupporting

confidence: 77%

The representation of peripheral nerve inputs in the S-I hindpaw cortex of rats raised with incompletely innervated hindpaws

Wall¹,

Cusick²

1986

J. Neurosci.

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The hindpaws of l-d-old rats were partially denervated by transection and ligation of the sciatic nerve. Following growth to adulthood, the topographical organization of the hindpaw representation in primary somatosensory (S-I) cortex was studied with neurophysiological mapping techniques and compared to the organization of previously studied normal adult rats and adult rats that had sciatic transection. The goals were (1) to determine how the topographical organization of the hindpaw representation is affected when development occurs with an incomplete set of peripheral inputs, and (2) to identify possible differences in the capacity of neonatal and adult CNSs to adjust to loss of inputs.The rat hindpaw is relatively immature on the day of birth. Neonatal transection and ligation of the sciatic nerve stunted gross development of the hindpaw and resulted in a permanent loss of low-threshold mechanoreceptor inputs from hindpaw zones normally innervated by the sciatic nerve.A comparison of the cortical representations of neonatally denervated and normal rats indicated that early loss of sciatic inputs caused several changes in the topographical organization of the hindpaw cortex, including (1) a loss of the representation of hindpaw skin areas innervated by the sciatic nerve, (2) a limited infringement of cutaneous inputs from the hindquarter into the cortical zone deprived of sciatic hindpaw inputs, (3) increased variability in the topographical relationships of the hindpaw and hindquarter representations, and (4) a decrease in the size of the cortical area responsive to cutaneous inputs.A comparison of the cortical representations of neonatal and adult denervates indicated that the general cortical reaction to sciatic injury at both ages was similar: Neurons in some parts of the deprived hindpaw cortex were activated by cutaneous inputs from uninjured nerves, whereas neurons in other parts of this cortex were unresponsive to cutaneous stimulation. The topographical organization and size of projection zones of uninjured peripheral inputs were different, however, after denervation in neonatal and adult rats.From these findings we suggest that (1) development of a normal, topographically organized hindpaw representation requires integration of hindpaw inputs in a spatially specific manner, (2) more than one pattern of cortical adjustment occurs after sciatic injury, and age is an important determinant of the pattern that is established, and (3) different mechanisms of central adjustment underlie age-related differences in cortical pat-

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Section: Present Jindingssupporting

confidence: 77%

The representation of peripheral nerve inputs in the S-I hindpaw cortex of rats raised with incompletely innervated hindpaws

Wall¹,

Cusick²

1986

J. Neurosci.

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“…The discrepancy in the severity of effects between birth-and adult-trimmed groups both in behavioral performance and in organization of M1 representations suggests that M1 displays a critical period of susceptibility to abnormal sensory feedback from the vibrissae. The structural and functional organization of rat S1 barrel cortex displays well characterized periods of susceptibility to a variety of peripheral manipulations (Kaas et al, 1983), including vibrissa trimming (Fox, 1992). S1 may therefore dictate the timing of such periods for both sensory and motor maps.…”

Section: Significancementioning

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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“…For example, in the cat visual system, retinal lesions lead to reorganization of cortical topography (3). Peripheral nerve sectioning can alter substantially the receptive fields of neurons in monkey somatosensory and motor cortices (6,7). Similarly, the directional tuning of neural receptive fields in monkey motor cortex changes as the animal learns to compensate for an externally applied force field while moving a manipulandum (8).…”

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confidence: 99%

An analysis of neural receptive field plasticity by point process adaptive filtering

Brown

Nguyen

Frank

et al. 2001

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

167

115

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Neural receptive fields are plastic: with experience, neurons in many brain regions change their spiking responses to relevant stimuli. Analysis of receptive field plasticity from experimental measurements is crucial for understanding how neural systems adapt their representations of relevant biological information. Current analysis methods using histogram estimates of spike rate functions in nonoverlapping temporal windows do not track the evolution of receptive field plasticity on a fine time scale. Adaptive signal processing is an established engineering paradigm for estimating time-varying system parameters from experimental measurements. We present an adaptive filter algorithm for tracking neural receptive field plasticity based on point process models of spike train activity. We derive an instantaneous steepest descent algorithm by using as the criterion function the instantaneous log likelihood of a point process spike train model. We apply the point process adaptive filter algorithm in a study of spatial (place) receptive field properties of simulated and actual spike train data from rat CA1 hippocampal neurons. A stability analysis of the algorithm is sketched in the Appendix. The adaptive algorithm can update the place field parameter estimates on a millisecond time scale. It reliably tracked the migration, changes in scale, and changes in maximum firing rate characteristic of hippocampal place fields in a rat running on a linear track. Point process adaptive filtering offers an analytic method for studying the dynamics of neural receptive fields.T he receptive fields of neurons are dynamic; that is, their responses to relevant stimuli change with experience. Experience-dependent change or plasticity has been documented in a number of brain regions (1-5). For example, in the cat visual system, retinal lesions lead to reorganization of cortical topography (3). Peripheral nerve sectioning can alter substantially the receptive fields of neurons in monkey somatosensory and motor cortices (6, 7). Similarly, the directional tuning of neural receptive fields in monkey motor cortex changes as the animal learns to compensate for an externally applied force field while moving a manipulandum (8). In the rat hippocampus, the system we study here, the pyramidal neurons in the CA1 region have spatial receptive fields. As a rat executes a behavioral task, a given CA1 neuron fires only in a restricted region of the experimental environment, termed the cell's spatial or place receptive field (9). Place fields change in a reliable manner as the animal executes its task (5, 10). When the experimental environment is a linear track, these spatial receptive fields on average migrate and skew in the direction opposite the cell's preferred direction of firing relative to the animal's movement and increase in scale and maximum firing rate (5, 10). Because receptive field plasticity is a characteristic of many neural systems, analysis of these dynamics from experimental measurements is crucial for understanding how different br...

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The Reorganization of Somatosensory Cortex Following Peripheral Nerve Damage in Adult and Developing Mammals

Cited by 611 publications

References 0 publications

The representation of peripheral nerve inputs in the S-I hindpaw cortex of rats raised with incompletely innervated hindpaws

The representation of peripheral nerve inputs in the S-I hindpaw cortex of rats raised with incompletely innervated hindpaws

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

An analysis of neural receptive field plasticity by point process adaptive filtering

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