Alterations in mechanoreceptor input to Brodmann's areas 1 and 3 of the postcentral hand area of Macaca mulatta after nerve section and regeneration

Paul, Ronald L.; Goodman, Herbert; Merzenich, Michael M.

doi:10.1016/0006-8993(72)90782-2

Cited by 72 publications

(22 citation statements)

References 9 publications

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“…Although no electrophysiological recordings were made in these TR patients, it is interesting to note that the character of the referred-touch sensations are reflective of receptive fields described in nerve section and repair studies (14,15). The large hand perceptions may result from the activation of anatomical connections between central pathways/cortical representations by a small number of randomly organized inputs from the skin surface (16)(17)(18)(19).…”

Section: Discussionmentioning

confidence: 93%

Redirection of cutaneous sensation from the hand to the chest skin of human amputees with targeted reinnervation

Kuiken

Marasco

Lock

et al. 2007

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

253

182

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Amputees cannot feel what they touch with their artificial hands, which severely limits usefulness of those hands. We have developed a technique that transfers remaining arm nerves to residual chest muscles after an amputation. This technique allows some sensory nerves from the amputated limb to reinnervate overlying chest skin. When this reinnervated skin is touched, the amputees perceive that they are being touched on their missing limb. We found that touch thresholds of the reinnervated chest skin fall within near-normal ranges, indicating the regeneration of largefiber afferents. The perceptual identity of the limb and chest was maintained separately even though they shared a common skin surface. A cutaneous expression of proprioception also occurred in one reinnervated individual. Experiments with peltier temperature probes and surface electrical stimulation of the reinnervated skin indicate the regeneration of small diameter temperature and pain afferents. The perception of an amputated limb arising from stimulation of reinnervated chest skin may allow useful sensory feedback from prosthetic devices and provides insight into the mechanisms of neural plasticity and peripheral regeneration in humans.regeneration ͉ neural machine interface ͉ touch ͉ artificial limbs T he loss of an arm is a singularly debilitating injury. Improving the function of artificial arms remains a considerable challenge, especially for high-level amputations where the disability is greatest. A primary impediment to better function is that current prostheses provide very little sensory feedback. The amputees must rely primarily on vision to manipulate objects, and they cannot feel what they touch with motorized prosthetic hands. This limitation greatly increases the cognitive burden on the amputee and impedes the use of the artificial limb.We have developed a neural-machine interface called targeted reinnervation (TR) that provides enhanced motor control and the potential for meaningful sensation feedback for artificial arms (1-3). The amputated brachial plexus nerves that once provided motor control and sensory feedback in the missing limb are transferred to arm and chest muscles that remain after the amputation. Once reinnervated, these muscles produce electromyogram (EMG) signals that correspond to the original arm control signals sent from the brain down the brachial plexus nerves. This process provides improved and more intuitive control of a motorized artificial arm (4-6). The contractions of the reinnervated muscles function as biological amplifiers for the motor commands transmitted by the amputated arm nerves. Concurrently, the sensory nerve fibers in these amputated nerves appear to reinnervate the skin overlying the target muscles. When this reinnervated skin is touched, the amputee feels as if the missing hand is being touched. This skin reinnervation may provide a direct portal to the sensory pathways of the amputated arm and hand. It could potentially provide an amputee with the ability to feel what he touches with a pro...

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Section: Discussionmentioning

confidence: 93%

Redirection of cutaneous sensation from the hand to the chest skin of human amputees with targeted reinnervation

Kuiken

Marasco

Lock

et al. 2007

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

253

182

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“…Perhaps accounting for some of the divergence in findings, different investigators used different criteria to classify neurons as SA1-or RA-like: in some studies, the distinction was based on the presence or absence of a sustained response to a step indentation (Paul et al 1972a;Sur et al 1981Sur et al , 1984. In other studies, neurons were classified on the basis of their SUSTAINED response and on their ability to produce entrained responses to vibratory stimuli in the high-flutter frequency range (50 -100 Hz) (Hyvärinen and Poranen 1978;Mountcastle et al 1969).…”

Section: Previous Studies Investigating Submodality Convergencementioning

confidence: 99%

Convergence of Submodality-Specific Input Onto Neurons in Primary Somatosensory Cortex

Pei

Denchev

Hsiao³

et al. 2009

Journal of Neurophysiology

100

119

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At the somatosensory periphery, slowly adapting type 1 (SA1) and rapidly adapting (RA) afferents respond very differently to step indentations: SA1 afferents respond throughout the entire stimulus interval (sustained response), whereas RA afferents respond only at stimulus onset (on response) and offset (off response). We recorded the responses of cortical neurons to step indentations and found many neurons in areas 3b and 1 to exhibit properties that are intermediate between these two extremes: These neurons responded during the sustained portion of the stimulus and also at the offset of the stimulus. Several lines of evidence indicate that these neurons, which exist in large proportions even at these early stages of somatosensory cortical processing, receive input from both populations of afferents. First, we show that many cortical neurons have both a significant sustained response and a significant off response. Second, the strength of the off response is uncorrelated with that of the sustained response, which is to be expected if sustained and off responses stem from different populations of afferent fibers. Third, the bulk of the variance in cortical responses to step indentations can be accounted for using a linear combination of both SA1 and RA responses. Finally, we show that the off response in cortical neurons does not reflect rebound from inhibition. We conclude that the convergence of modality specific input onto individual neurons is common in primary somatosensory cortex and discuss how this conclusion might be reconciled with previous findings.

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“…Results from other somatosensory systems have reported changes in the dorsal horn or dorsal column nuclei after section of the hind-limb or forelimb nerves (Devor & Wall, 1978 a, b; Kalaska & Pomeranz, 1982) or dorsal roots (Pubols & Goldberger, 1980;Millar, Basbaum & Wall, 1976; Dostrovsky, Millar & Wall, 1976). Also cortical changes occur after neonatal (Kelahan, Ray, Carson, Massey & Doetsch, 1981) or adult (Rasmusson, 1982) digit amputation or section of sensory nerves to the hand in kittens and adult cats (Kalaska & Pomeranz, 1979) and young or adult monkeys (Paul, Goodman & Merzenich, 1972;Merzenich, Kaas, Nelson, Wall, Sur & Felleman, 1980). However, only very limited plasticity was found here after adult lesions, compared to marked changes after lesions in neonates.…”

Section: Introductionmentioning

confidence: 99%

Rearrangement of neuronal responses in the trigeminal system of the rat following peripheral nerve section.

Waite¹

1984

The Journal of Physiology

118

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SUMMARY1. The infraorbital nerve was cut in either neonatal (on day 0) or adult (day 60) rats and the peripheral regeneration prevented. After 60 days either anatomical or electrophysiological techniques were used to study the peripheral nerve, trigeminal nucleus and somatosensory cortex.2. In neonatally sectioned animals the number of myelinated fibres surviving, at 60 days, in the peripheral nerve proximal to the lesion was 11 % compared with 100 % survival after adult nerve section.3. This reduction in surviving nerve fibres in neonatally lesioned animals was associated with a significant reduction in cross-sectional area of all trigeminal nuclei (principalis, oralis, interpolaris and caudalis) of 18-29 %. No significant change in area was present in animals sectioned as adults.4. Neonatally lesioned animals also showed a reduction of approximately 20% in the number of cells visible in cross-sections of all trigeminal nuclei.5. Animals sectioned as neonates showed marked plasticity at all nuclei in the trigeminal complex as well as in the cortex. Deafferented cells responded to new peripheral receptive fields so that the somatotopic organization of these cells was modified. Such cells are referred to throughout as 'reactivated' cells. However, in animals sectioned as adults no evidence of plasticity could be detected in the trigeminal nuclei. Only very limited reactivation was apparent in the cortex, so that the majority of deafferented cells remained unresponsive at both sites. 6. A detailed comparison was made of twenty-three reactivated cells and twentyfive normal cells from nucleus principalis of animals with nerve section on day 0. The reactivated cells commonly showed larger, more complex receptive fields, longer latencies and lower following frequencies, although stimulus thresholds were similar. Thus reactivated cells showed more convergence and poorer synaptic security than normal cells. However, stimulation of the contralateral thalamus produced similar responses from both groups of cells, suggesting that not all inputs to reactivated cells were modified.7. The time course of the reactivation of cells in nucleus caudalis from animals lesioned on day 0 was followed over 30 days. No acute effect, for up to 24 h, was detected. However, somatotopic reorganization had started by day 7, proceeded rapidly between days 7 and 14, and was completed by day 21.

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Alterations in mechanoreceptor input to Brodmann's areas 1 and 3 of the postcentral hand area of Macaca mulatta after nerve section and regeneration

Cited by 72 publications

References 9 publications

Redirection of cutaneous sensation from the hand to the chest skin of human amputees with targeted reinnervation

Redirection of cutaneous sensation from the hand to the chest skin of human amputees with targeted reinnervation

Convergence of Submodality-Specific Input Onto Neurons in Primary Somatosensory Cortex

Rearrangement of neuronal responses in the trigeminal system of the rat following peripheral nerve section.

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