Comparative study of the neuronal plasticity along the neuraxis of the vibrissal sensory system of adult rat following unilateral infraorbital nerve damage and subsequent regeneration

Abstract

The aim of the present study was to examine the physiological consequences of a unilateral infraorbital nerve lesion and its regeneration at different levels of the somatosensory neuraxis. In animals whose right infraorbital nerve had been crushed, a large unresponsive area was found in the main brainstem trigeminal nucleus (Pr5). Responses evoked by ipsilateral vibrissal deflection in the middle of Pr5 reappeared only on days 22-35 after the nerve had been transected, whereas recovery from the nerve crush took only 7-9 days. However, no sign of short-term neuronal plasticity was observed in Pr5 after peripheral nerve injury. An enlargement of the receptive fields in two-thirds of the units and a lengthening in the delay of the evoked responses were observed as long-term plastic changes in Pr5 neurons after peripheral-nerve regeneration. In the ventral posteromedial nucleus of the thalamus (VPM) of partly denervated animals, however, only minutes or hours after the nerve crush, certain units were found to respond in some cases not only to the vibrissae, but also to mechanical stimulation of the face over the eye (two units), the nose (one unit), and the midline (one unit). Apart from the experiments involving incomplete denervation, the vibrissal representation areas of the VPM were unresponsive to stimulation of both the vibrissae and other parts of the face until nerve regeneration had occurred. In the somatosensory cortex, an infraorbital nerve crush immediately resulted in a large cortical area being unresponsive to vibrissal deflection. It was noteworthy, however, that shortly after the nerve crush, this large unresponsive whisker representation cortical area was invaded from the rostromedial direction by responses evoked by stimulation of the forepaw digits. In spite of the reappearance of vibrissa-evoked responses 7-10 days after the nerve crush, an expanded digital representation could still be observed 3 weeks after the nerve crush, resulting in an overlapping area of digital and vibrissal representations. The withdrawal of the expanded representation of forepaw digits was completed by 60 days after the nerve crush. The results obtained in Pr5, the VPM, and the cortex strongly suggest that the higher the station in the neuraxis, the greater the degree of plasticity after infraorbital nerve injury.

Response properties of whisker-associated primary afferent neurons following infraorbital nerve transection with microsurgical repair in adult rats

“…A likely explanation is that a regenerating axon follows a channel, possibly established by Schwann cells distal to the transection (Fawcett and Keynes 1990), which leads to a single whisker follicle. The misrouting of regenerating distal axons will have a substantially deleterious effect on CNS processing that depends on high-resolution spatial mapping (Kis et al 1999;Waite and Cragg 1982).…”

Neuron numbers in the sensory trigeminal nuclei of the rat: A GABA‐ and glycine‐immunocytochemical and stereological analysis

“…Rather than subsiding, however, the interest in furthering the anatomical knowledge of these nuclei expanded considerably more recently, with the trigeminal system becoming a model to study development and neural pattern formation Waite and De Permentier, 1997), sensory information processing (Szwed et al, 2003;Jones et al, 2004), sensorimotor integration (Tsuboi et al, 2003), and neural plasticity (Melzer and Smith, 1998;Kis et al, 1999;Machín et al, 2004), to develop models of pain (Vos et al, 2000), or to design artificial sensors in robotics (Fend et al, 2003).…”

An Index of Topographic Normality in Rat Somatosensory Cortex: Application to a Sciatic Nerve Crush Model

“…In general, it has been shown that nerve crush injuries result in fewer reinnervation errors than repaired nerve cut injuries and are associated with good recovery (Wall et al 1983). The index of topography and the cutaneous threshold measures used in this study were employed to establish a more precise, quantitative measure of physiological recovery from nerve crush injuries (Kawakami et al 1989;Kis et al 1999;Korodi and Toldi 1998). These quantitative measures allow for statistical comparisons between various nerve repair techniques (e.g., end-to-end repair versus tubulization) (see Lundborg et al 1997;Meyer et al 1997) and possible rehabilitative therapies (e.g., Florence et al 2001;Xerri et al 1998).…”

“…Several studies have shown that minor regeneration errors do occur following nerve crush injuries (Munger and Renehan 1989;Povlsen et al1994;Sanders and Zimmerman 1986) and that these errors can distort cortical topography (Kawakami et al 1989;Kis et al 1999;and Korodi and Toldi 1998). The implication of these earlier studies is that cutaneous sensitivity in the reinnervated skin territories may be compromised by nerve crush injury.…”