Reorganization of mammalian somatosensory cortex following peripheral nerve injury

doi:10.1016/0166-2236(82)90235-1

Trends in Neurosciences

Volume 5, 1982, Pages 434-436

https://doi.org/10.1016/0166-2236(82)90235-1 Get rights and content

Abstract

It is now clear that the adult mammalian somatosensory system is capable of very significant functional reorganization after peripheral-nerve or spinal-cord injury. When, by sectioning either a peripheral nerve or the sensory tracts within the spinal-cord, neurons in the spinal cord^1–4, dorsal-column nuclei¹¹, thalamus¹⁶ and cortex^{6,7,9,10,12–14} are deprived of their normal activating input, they can become responsive to the stimulation of new parts of the body surface. This functional (though not necessarily connectional) plasticity, involving apparent reorganization of topographic maps, was unexpected in a mature sensory system with (presumably) fully established central connections. Thus these changes in central somatotopic organization suggest that either the effectiveness of previously existing synapses can be modified dramatically, or that new connections and synapses may be formed in a topographically controlled manner — perhaps both these processes occur. The mechanisms involved in this reorganization almost certainly reflect those responsible for the development and active maintenance of normal sensory-system organization. We have concentrated our investigations on reorganization of somatosensory cortex because it is easier to study the large and very accessible cortical representations, and because cortical maps should reflect many of the alterations occurring within the sub-cortical projection system.

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Spinal cord injury is a devastating condition that haunts human lives. Typically, patients experience referred phantom sensations on the hand when they are touched on the face. In adult monkeys, massive deafferentations such as chronic dorsal column lesions at higher cervical levels result in the large-scale expansion of face inputs into the deafferented hand cortex of area 3b. However, adult rats with thoracic dorsal column lesions do not demonstrate such large-scale reorganization. The large-scale face expansion in area 3b of monkeys is driven by the reorganization of the cuneate nucleus in the medulla. The sprouting of afferents from the trigeminal nucleus to the adjacent deafferented cuneate nucleus is facilitated by close proximity and compactness of the medulla in primates. Previously, in adult rats with thoracic lesions, the cuneate nucleus was not deafferented and its functional organization was not explored. The extent of the deafferentation and the duration of the recovery period are two major factors that determine the extent of reorganization. Hence, higher cervical (C3-C4) dorsal column lesions were performed, which cause massive deafferentations, and physiological maps were obtained after prolonged recovery periods (3 weeks −18 months). In spite of the above, the expansion of the intact face inputs was not observed in the deafferented zones of the primary somatosensory cortex (SI) and medulla of adult rats. The deafferented forelimb and hindlimb representations in SI were unresponsive to cutaneous stimulation of any part of the body. The cuneate and gracile nuclei in rats with complete dorsal column lesions remained mostly inactive except for a few sites which responded to stimulation of the spared upper arm. Hence, dorsal column lesions have different effects on the adult primate and rodent somatosensory systems. Appreciating this inter-species difference can aid in identifying the underlying neural substrates and restrict maladaptive reorganizations to cure phantom sensations.
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Due to the complexity of the afferents contained within a particular DRG, selecting the correct target for stimulation may require more than simply relying on a dermatomal map. In cases like post-amputation pain (PAP), maladaptive changes occur within the central nervous system (55–57) such that a lead placed over the L5 DRG may not correspond to the phantom foot due to deafferentation and central sensitization (57–60). Currently there is debate whether phantom limb pain is a top-down phenomenon due to loss of sensory input and caused by maladaptive cortical plasticity or a bottom-up phenomenon due to exaggerated input in the primary afferent neurons in the DRG innervating that limb (61).
The Neuromodulation Appropriateness Consensus Committee (NACC) is dedicated to improving the safety and efficacy of neuromodulation and thus improving the lives of patients undergoing neuromodulation therapies. With continued innovations in neuromodulation comes the need for evolving reviews of best practices. Dorsal root ganglion (DRG) stimulation has significantly improved the treatment of complex regional pain syndrome (CRPS), among other conditions. Through funding and organizational leadership by the International Neuromodulation Society (INS), the NACC reconvened to develop the best practices consensus document for the selection, implantation and use of DRG stimulation for the treatment of chronic pain syndromes.
The NACC performed a comprehensive literature search of articles about DRG published from 1995 through June, 2017. A total of 2538 article abstracts were then reviewed, and selected articles graded for strength of evidence based on scoring criteria established by the US Preventive Services Task Force. Graded evidence was considered along with clinical experience to create the best practices consensus and recommendations.
The NACC achieved consensus based on peer-reviewed literature and experience to create consensus points to improve patient selection, guide surgical methods, improve post-operative care, and make recommendations for management of patients treated with DRG stimulation.
The NACC recommendations are intended to improve patient care in the use of this evolving therapy for chronic pain. Clinicians who choose to follow these recommendations may improve outcomes.
Selective Radiofrequency Stimulation of the Dorsal Root Ganglion (DRG) as a Method for Predicting Targets for Neuromodulation in Patients With Post Amputation Pain: A Case Series
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This presents a potential problem in using DRG for PAP as the pain patterns may not conform to simple dermatomal patterns due to the maladaptive changes known to occur in the central nervous system after the amputation (25–27). As such a patient with phantom foot pain may not respond to a lead placed over the L5 DRG simply due to the dermatomal representation of the foot due to severe deafferentation or centralization of the pain (27–30). This can be potentially problematic for a patient undergoing a DRG SCS trial, leading to trial failure for no other reason than inability to provide relief to the area of need.
While spinal cord stimulation (SCS) has established itself as an accepted and validated treatment for neuropathic pain, there are a number of conditions where it has experienced less, long-term success: post amputee pain (PAP) being one of them. Dorsal root ganglion (DRG) stimulation has shown great promise, particularly in conditions where traditional SCS has fallen short. One major difference between DRG stimulation and traditional SCS is the ability to provide focal stimulation over targeted areas. While this may be a contributing factor to its superiority, it can also be a limitation insofar stimulating the wrong DRG(s) can lead to failure. This is particularly relevant in conditions like PAP where neuroplastic maladaptation occurs causing the pain to deviate from expected patterns, thus creating uncertainty and variability in predicting targets for stimulation. We propose selective radiofrequency (RF) stimulation of the DRG as a method for preoperatively predicting targets for neuromodulation in patients with PAP.
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In each patient, stimulating one or more DRG(s) produced paresthesias patterns that were contradictory to know dermatomal patterns. Upon completion of a one-week trial all four patients reported 60–90% pain relief, with coverage over the painful areas, and opted for permanent implant.
Mapping the DRG via RF stimulation appears to provide improved accuracy for determining lead placement in the setting of PAP where pain patterns are known to deviate from conventional dermatomal mapping.
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This chapter summarizes experiments showing that deprivation of somatosensory input could also elicit organizational changes in the hemisphere contralateral to the deafferented one. The existence of interactions among homotopic sites within cortical representations in both hemispheres provides a substrate for such an effect. It has been proposed that chronic deafferentation, in association with long-term practice as in blind, deaf, or individuals with amputation results in compensatory gains in the same and in other sensory modalities. However, the long-term changes described are mild and the question whether blind or deaf people develop enhanced capacities of their remaining senses is still controversial. Acute deafferentation leads to rapid changes of contra and ipsilateral cortical representations. Much less is known about the behavioral consequences of acute deafferentation in humans. It is conceivable that there are “built-in” mechanisms by which interruption of sensory input from one region leads to perceptual compensatory enhancements in a different site. An immediate behavioral improvement in a different body site or modality following acute deafferentation could reflect the existence of compensatory mechanisms to allow coping with the new deficit.

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¹: M. M. Merzenich is Professor of Otolaryngology and Physiology, University of California at San Francisco, San Francisco CA, 94143, U.S.A.

²: J. H. Kaas is Professor of Psychology, Vanderbilt University, Nashville, TN 37240, U.S.A.

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Trends in Neurosciences

ReviewReorganization of mammalian somatosensory cortex following peripheral nerve injury

Abstract

Exp. Neurol.

Brain Res.

Brain Res.

Nature (London)

J. Neuroscience

J. Comp. Neurol.

Science

J. Neurophysiol.

Review
Reorganization of mammalian somatosensory cortex following peripheral nerve injury