Reorganization of sensory modalities evoked by microstimulation in region of the thalamic principal sensory nucleus in patients with pain due to nervous system injury

Abstract

Stimulation of the somatosensory system is more likely to evoke pain in patients with chronic pain after nervous system injury than in patients without somatosensory abnormalities. We now describe results of stimulation through a microelectrode at microampere thresholds (threshold microstimulation; TMIS) in the region of the human thalamic principal sensory nucleus (ventral caudal; Vc) during operations for treatment of movement disorders or of chronic pain. Patients were trained preoperatively to use a standard questionnaire to describe the location (projected field) and quality of sensations evoked by TMIS intraoperatively. The region of Vc was divided on the basis of projected fields into areas representing the part of the body where the patients experienced chronic pain (pain affected) or did not experience chronic pain (pain unaffected) and into a control area located in the thalamus of patients with movement disorders and no experience of chronic pain. The region of the Vc was also divided into a core region and a posterior-inferior region. The core was defined as the region above a standard radiologic horizontal line (anterior commissure-posterior commissure line; ACPC line) where the majority of cells responded to innocuous somatosensory stimulation. The posterior-inferior area was a cellular area posterior and inferior to the core. In both the core and the posterior-inferior regions, the proportion of sites where TMIS evoked pain was larger in pain-affected and unaffected areas than in control areas. The number of sites where thermal (warm or cold) sensations were evoked was correspondingly smaller, so that the total of pain-plus-thermal (sensation of warmth or cold) sites was the same in all areas. Therefore, sites pain where stimulation evoked pain in patients with neuropathic pain (i.e., pain following an injury to the nervous system) may correspond to sites where thermal sensations were evoked by stimulation in patients without somatosensory abnormality.

Lesions Limited to the Human Thalamic Principal Somatosensory Nucleus (Ventral Caudal) Are Associated with Loss of Cold Sensations and Central Pain

“…Involvement of Vc and S1 is consistent with hypersensitivity to electrical stimulation of Vc and primary somatic sensory cortex, which produce pain more commonly in patients with central pain than those without (Katayama et al, 1994;Davis et al, 1996;Lenz et al, 1998;Nguyen et al, 2000;Brown and Barbaro, 2003).…”

Deconstructing Central Pain with Psychophysical and Neuroimaging Studies

“…Thus, this latter report does not speak directly to the mechanism of central pain. Electrical stimulation in the area of Vc evoked pain more commonly in central pain patients with allodynia, versus those without allodynia (Lenz et al, 1998;Davis et al, 1996). Overall, these studies suggest that reorganization of the region of Vc contributes to the symptoms of central pain.…”

“…In both studies, a combined cold and mechanical cutaneous stimulus produced allodynia, and was associated with intense bloodflow activation of contralateral sensorimotor (frontal and parietal) cortex. In addition, pain sensations are evoked in subjects with CPSP by electrical stimulation of S1 cortex (Katayama et al, 1994;Nguyen et al, 2000;Brown and Barbaro, 2003) or of thalamic nucleus Vc, which projects to it (Lenz et al, 1998;Davis et al, 1996). Lesions of parietal cortex can dramatically relieve pain in subjects with CPSP resulting from thalamic lesions (Soria and Fine, 1991;Helmchen et al, 2002;Canavero and Bonicalzi, 2007).…”

Cross-modal plasticity in the human thalamus: evidence from intraoperative macrostimulations

“…Fewer studies addressed other aspects, like plasticity, and these were focused on lateral, somatosensory nuclei (Lenz et al 1995(Lenz et al , 1998Lenz and Byl 1999). In the present study, the large number of stimulations performed during stereotactic operations in patients with different syndromes provides a unique opportunity to examine the distribution of response modalities in the human thalamus and their relation to different pathologies.…”

“…Microelectrode recordings and stimulations in patients with different functional disorders have already provided evidence for abnormal activities in both lateral and medial thalamus (Lenz et al 1989;Jeanmonod et al 1994Jeanmonod et al , 1996Magnin et al 2000), as well as alterations in receptive field representations and somatotopic organization in the lateral thalamus after nerve injury such as limb amputation (Lenz et al 1994(Lenz et al , 1998Hua et al 2000;Ohara and Lenz 2001; see also Anderson et al 2006). These plastic changes resemble those observed in the human somatosensory cortex (Flor et al 1998;Elbert and Rockstroh 2004), as well as those well recognized at cortical and subcortical levels in non-human primates and present also in other cortical sensory and motor areas (Garraghty and Kaas 1991;Kaas 1991;Buonomano and Merzenich 1998;Florence et al 2000;Merzenich 2002).…”