Chronic electrical stimulation of transected peripheral nerves preserves anatomy and function in the primary somatosensory cortex

Abstract

The structure and function of the central nervous system strongly depend on the organization and efficacy of the incoming sensory input. A disruption of somesthetic input severely alters the metabolic activity, electrophysiological properties and even gross anatomical features of the primary somatosensory cortex. Here we examined, in the rat somatosensory cortex, the neuroprotective and therapeutic effects of artificial sensory stimulation after irreversible unilateral transection of a peripheral sensory nerve (the infraorbital branch of the trigeminal nerve). The proximal stump of the nerve was inserted into a silicon tube with stimulating electrodes, through which continuous electrical stimulation was applied for 12 h/day (square pulses of 100 μs, 3.0 V, at 20 Hz) for 4 weeks. Deafferented animals showed significant decreases in cortical evoked potentials, cytochrome oxidase staining intensity (layers II-IV), cortical volume (layer IV) and number of parvalbumin-expressing (layers II-IV) and calbindin-D28k-expressing (layers II/III) interneurons. These deafferentation-dependent effects were largely absent in the nerve-stimulated animals. Together, these results provide evidence that chronic electrical stimulation has a neuroprotective and preservative effect on the sensory cortex, and raise the possibility that, by controlling the physical parameters of an artificial sensory input to a sectioned peripheral nerve, chronically deafferented brain regions could be maintained at near-'normal' conditions. Our findings could be important for the design of sensory neuroprostheses and for therapeutic purposes in brain lesions or neural degenerative processes.

Long-Term High-Level Exercise Promotes Muscle Reinnervation With Age

“…We further speculate that high-level activity either by voluntary exercise or functional electrical stimulation may be applied at any age to save neurons from disorders secondary to inactivity (55) and to counteract muscle atrophy in other neuromuscular or metabolic diseases (56). We further speculate that high-level activity either by voluntary exercise or functional electrical stimulation may be applied at any age to save neurons from disorders secondary to inactivity (55) and to counteract muscle atrophy in other neuromuscular or metabolic diseases (56).…”

Substitution of natural sensory input by artificial neurostimulation of an amputated trigeminal nerve does not prevent the degeneration of basal forebrain cholinergic circuits projecting to the somatosensory cortex

“…Our experimental model is the irreversible transection of the infraorbital nerve associated to a neuroprosthetic microdevice for stimulation of the proximal stump (Herrera-Rincon et al, 2012 ). Briefly, after complete transection of the peripheral nerve the proximal stump is inserted in a neuroprosthetic microdevice made by a silicon implant containing the electrodes that are externalized through the scalp and connected to an external stimulation device (CYGNUS-PG4000, Cygnus Tech, Delaware Water Gap, PA, USA) by means of circular connectors (Nano Circular Series; Omnetics® Connector Corporation, MN, USA) attached to the skull.…”

“…In a previous work we quantified cortical plasticity phenomena in young adult rats submitted to infraorbital nerve transection and subsequent artificial electrical neurostimulation (Herrera-Rincon et al, 2012 ). Sensory deprivation resulted in a clear decrease of the electrophysiological responses, metabolic activity, volume of the active neural tissue, and number of Parvalbumin- and Calbindin-positive GABA-ergic neurons, all of them consistent with previous literature (Land and Simons, 1985 ; Diamond et al, 1994 ; Glazewski et al, 1998 ; Huang et al, 1998 ; Kelly et al, 1999 ; Machin et al, 2004 ; for review, see Fox, 2002 ).…”

“…Sensory deprivation resulted in a clear decrease of the electrophysiological responses, metabolic activity, volume of the active neural tissue, and number of Parvalbumin- and Calbindin-positive GABA-ergic neurons, all of them consistent with previous literature (Land and Simons, 1985 ; Diamond et al, 1994 ; Glazewski et al, 1998 ; Huang et al, 1998 ; Kelly et al, 1999 ; Machin et al, 2004 ; for review, see Fox, 2002 ). However, all these physiological alterations, both functional and metabolic, were prevented or significantly diminished when the peripheral nerve was chronically stimulated after the transection (Herrera-Rincon et al, 2012 ).…”

Sensory Input-Dependent Changes in Glutamatergic Neurotransmission- Related Genes and Proteins in the Adult Rat Trigeminal Ganglion

“…Primary sensory neurons directly affected by axotomy or other nerve injuries display a multitude of cellular and molecular reactions that to a large extent reveal a self-protective and regenerative response (Fu and Gordon, 1997; Xiao et al, 2002; Lawson, 2005). Further upstream in the sensory pathway, however, neural changes reflect a combination of effects, those due to transsynaptic effects of deafferentation, and others resulting from the loss or distortion of the afferent input (Matthews, 1964; Panetsos et al, 2008; Herrera-Rincon et al, 2012). Both types of effects often, but not always, result in overlapping phenotypic changes in higher sensory centers.…”