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Primary somatosensory cortex in rats with pain-related behaviours due to a peripheral mononeuropathy after moderate ligation of one sciatic nerve: neuronal responsivity to somatic stimulation

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Summary

Single-unit recordings were made under moderate gaseous anaesthesia in the hindpaw representation area of the two primary somatosensory motor cortices (SmI) of rats (n = 58) rendered mononeuropathic by four loose ligatures placed around one common sciatic nerve 2–3 weeks beforehand. The rats exhibited clear hyperalgesia and allodynia from the paw with the ligated sciatic nerve, to both mechanical and thermal stimuli. From the tested neuronal population (n = 640), about the same proportion could be activated by somatic stimuli in each cortex: 165/362 (45%) in the cortex contralateral to the ligated sciatic nerve (Cc), 105/278 (37%) in the cortex ipsilateral to the ligated sciatic nerve (Ci). Neurones driven by light touch, exhibited RFs strictly contralateral to the recording sites. Their proportion and response characteristics were similar regardless of recording side. However, the number of neurones with RFs in the sciatic nerve territory was above 95% in the Ci, and was dramatically reduced to 43 % in the Cc. By contrast, the number of neurones with RFs supplied by the saphenous nerve reached 57% on this side. Although the RF size of all the neurones appeared roughly normal, there were fewer Cc than Ci neurones with RFs located on the paw itself and with RFs of extremely small size in the sciatic nerve territory. The proportion of neurones responding to a joint stimulus was significantly higher in the Cc than in the Ci. The neuronal responses to joint stimuli of the paw with the ligated sciatic nerve were significantly more sustained than those recorded in the Ci and elicited from the normal paw. The proportion of neurones driven by mechanical stimulation which gave rise to nociceptive reactions in freely moving animals, i.e. “nociceptive” neurones, was comparable in each cortex. However, half of the Cc neurones exhibited paroxysmal discharges occuring without intentional stimulation and of long duration (l min to several minutes). Only 66% of Cc but 93% of Ci “nociceptive” neurones were exclusively activated by pinch. The remaining Cc neurones were also activated by applying moderate pressure to the paw with the ligated nerve. Pinch responses from the paw with the ligated nerve were often more intense and of longer duration than responses elicited from the intact paw. The “nociceptive” Cc neurones were especially sensitive to thermal stimuli of 39–44° C when the stimuli were applied to the paw with the ligated nerve. They also responded vigorously to a 10° C stimulus applied to this paw. They were therefore, sensitive to thermal stimuli usually considered to be in the non-noxious range. In the SmI cortex opposite to the ligated sciatic nerve, there was no change in the proportion of somatosensory neurones, but a rearrangement of the various somatic inputs. Although reduced, there were consistent light tactile inputs from the damaged sciatic nerve giving rise to roughly normal neuronal responses, and simultaneously a noticeable increase in tactile signals from the saphenous nerve territory. There was also a significant increase in joint inputs from the paw with the ligated sciatic nerve. The possible functional role of such input rearrangement is discussed. The dramatic changes in the responses of “nociceptive” neurones to stimuli applied to the paw with the ligated sciatic nerve and the clear decrease in their activation threshold to mechanical and thermal stimuli could account for some of the abnormal pain-related behaviours that were exhibited. These data emphasize, again, that the primary sensory cortex is involved in nociceptive processing.

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  1. A. Levante

    Present address: Department of Anaesthesia, Hôpital Lariboisière, Paris, France

  2. J. C. Willer

    Present address: Explorations Fonctionnelles Neurologiques, Hôpital de la Salpêtriére, Paris, France

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  1. Unite de Recherches de Physiopharmacologie du Systéme Nerveux (U 161), Institut de la Santé et de la Recherche Medicale, 2 Rue d'Alésia, F-75014, Paris, France

    G. Guilbaud, J. M. Benoist, A. Levante, M. Gautron & J. C. Willer

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Guilbaud, G., Benoist, J.M., Levante, A. et al. Primary somatosensory cortex in rats with pain-related behaviours due to a peripheral mononeuropathy after moderate ligation of one sciatic nerve: neuronal responsivity to somatic stimulation. Exp Brain Res 92, 227–245 (1992). https://doi.org/10.1007/BF00227967

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