Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus

Abstract

The activity of 132 neurons in the caudal part of the ventral posterior lateral nucleus (VPLc) of the thalamus was recorded from 23 anesthetized monkeys. All single thalamic units that could be excited by electrical search stimuli applied to the contralateral sciatic nerve were investigated. Responses of these cells to mechanical, thermal, and electrical stimuli applied in the periphery indicated that at least half of the sampled cells were nociceptive. Based on responses to graded mechanical stimuli applied to the periphery, 110 of the sampled cells that received a predominant input from cutaneous receptive fields were classified. There were 56 low-threshold, 39 wide dynamic range, and 15 high-threshold cells. The same neurons were also classified into five mechanical types based on a cluster analysis: types 1-5 contained 25, 34, 17, 10, and 24 cells, respectively. The fact that about half the population of cells belonged to either the wide dynamic or the high threshold group (or mechanical types 3-5) suggested that a large population of VPLc neurons respond to mechanical nociceptive stimuli either exclusively or preferentially. Responses of 63 thalamic neurons were tested to noxious heat pulses applied to their cutaneous receptive fields with a contact thermostimulator. Of these, 47 cells were excited, whereas only 16 cells did not respond. The peripheral nerve that innervated the receptive field of each of 82 thalamic neurons was stimulated with graded strengths to activate A fibers only or both A and C fibers. All tested cells responded to peripheral A fiber volleys. In addition, 42 of these cells responded to peripheral C fiber volleys. The C fiber responses could be either short lasting (a few hundreds of milliseconds) or long lasting (up to several seconds). The recording sites of 80 cells were reconstructed. Of these, 78 were in the VPLc nucleus and the remaining two were in the reticular nucleus of the thalamus. No obvious relationship between the response characteristics and the locations of the cells within the VPLc nucleus was found. Sampled thalamic units had a variety of sources of input from the periphery, including both cutaneous and/or deep tissue receptive fields. The majority of the cells, however, had exclusively cutaneous receptive fields. The sizes of the cutaneous receptive fields were often very small, so that nearly half (41%) of the receptive fields of cells sampled occupied an area of skin smaller than half the foot.(ABSTRACT TRUNCATED AT 400 WORDS)

Squirrel monkey lateral thalamus. I. Somatic nociresponsive neurons and their relation to spinothalamic terminals

“…The overall somatotopic organization of VP agrees with earlier studies (Kaas et al, 1984;Chung et al, 1986). However, the receptive field sizes of LT and nociresponsive neurons in VP Cel l s that were found at a distance greater than 100 pm from spinothalamic terminals (-) are assumed to be unable to receive spinothalamic inputs.…”

“…Nociresponsive cells in thermoceptive cells were recently described in VPM of the awake the macaque are also scattered within the core of VPL and the behaving macaque (Bushnell et al, 1993). These units, WDR majority are WDR type (Chung et al, 1986). However, using type and NS type, were found concentrated along the borders an electrical search stimulus, Chung et al report a higher inciof VPM.…”

“…This difference is likely due to the different recording strategies used, Kaas et al continuously mapped multiunit responses while we only studied wellisolated individual neurons. The proportion of nociresponsive cells encountered in the thalamus seems to vary with the species used, for example, rat (Guilbaud et al, 1980), cat (Kniflki andMartin et al, 1990), and monkey (Chung et al, 1986); search stimulus employed; and the region of the thalamus examined (Dong et al, 1978;Chung et al, 1986;Briiggemann et al, 1993, in press). Thus, generalizations on the subject are hard.…”

“…These studies show important species differences in the location and topography of these neurons in the lateral thalamus. Nociresponsive cells have been described in the core of the ventral posterior complex (VP) in both rat and monkey and the large majority of these are wide-dynamic-range type (WDR, Guilbaud et al, 1980;Kenshalo et al, 1980;Chung et al, 1986;Casey and Morrow, 1987). On the other hand, nociresponsive cells in the cat seem to be confined to the ventral and dorsal border regions of this region (VP is designated as ventrobasal complex in cat and raccoon; Honda et al, 1983;KnilIki and Mizumuna, 1983;KnilIki and Craig, 1985;Yokota et al, 1988).…”

A PET activation study of dynamic mechanical allodynia in patients with mononeuropathy

“…A study of primates with a damaged primary somatosensory cortex and a case report of a patient with a tumor affecting the secondary somatosensory cortex have revealed clear de®cits in pain discrimination (Kenshalo et al, 1991;Greenspan and Win®eld, 1992) which supports the hypothesis that the lateral pain system plays an important role in the sensory/discriminative aspects of pain processing (Kenshalo et al, 1980;Kenshalo and Isensee, 1983;Albe-Fessard et al, 1985;Chung et al, 1986;Friedman and Murray, 1986;Vogt et al, 1993;Apkarian and Shi, 1994;Willis, 1995). Several functional imaging studies of phasic heat pain, tonic pain and electrically induced pain support the involvement of S1, S2 and the thalamus in pain processing (Talbot et al, 1991;Casey et al, 1994;Coghill et al, 1994;Hsieh, 1995; (Talairach and Tournoux, 1988).…”