Characteristics of somatotopic organization and spontaneous neuronal activity in the region of the thalamic principal sensory nucleus in patients with spinal cord transection

1. We explored the region of the principal sensory nucleus of thalamus (Vc) during stereotactic surgical procedures for treatment of patients with pain after spinal cord transection (spinal patients, n = 5) or of patients with movement disorders (n = 23). Receptive fields (RFs) of thalamic single neurons and locations of sensations evoked by stimulation (projected field, PF) were determined by standard methods. The cellular thalamic region where sensations were evoked at <25 μA was termed the 'region of Vc.' The region of Vc in spinal patients was subdivided into different areas according to RF and PF locations. Areas that were distant from the representation of the anesthetic part of the body were termed 'spinal control' areas, whereas those that were adjacent to or included in the representation of the area of absolute sensory loss were termed 'border zone/anesthetic' areas. The region of Vc in movement disorder patients were termed the 'control' area. 2. Border zone/anesthetic areas of thalamus often exhibited increased representations of the border of the anesthetic part of the body in comparison with the representation of the same parts of the body in control and spinal control areas. 3. In control and spinal control areas the locations of RFs and PFs were usually well matched. However, in border zone/anesthetic areas of the thalamus there was frequently a mismatch between the location of RFs and PFs (RF/PF mismatch). In border zone/anesthetic areas, RFs were often located on the border of the anesthetic part of the body whereas PFs were referred to anesthetic parts of the body. 4. Analysis of first- and higher-order properties of spontaneous neuronal activity revealed that spike trains could be classified into two groups with distinct patterns of activity. The R group (n = 49) was characterized by independence of sequential interspike intervals (ISIs), a Poisson distribution of ISIs, initially inhibitory or flat autocovariance function (acvf), and low level of high-frequency bursting. The O group (n = 26) was characterized by correlation of sequential ISIs, large sustained postspike facilitation on the acvf, and high prevalence of high- frequency bursting-all consistent with a bursting pattern of activity. A third group of spike trains (n = 17) had an initially inhibitory or flat acvf and a unimodal, positively shifted, ISI distribution that did not meet criteria for a Poisson distribution. 5. Spike trains in the R group were much more common in control and control spinal areas, whereas those in the O group were more common in border zone/anesthetic areas. 6. We carried out detailed analysis for bursts of the type associated with the occurrence of calcium spikes. Bursts of this type, particularly those composed of four or more ISIs, were much more common in the spike trains of cells located in border zone/anesthetic areas that did not have RFs. These spike trains were associated with a lower rate of action potentials occurring outside bursts, suggesting that decreased tonic excitatory levels were associated with the bursting activity of these cells. 7. All spinal patients experienced pain or dysesthesias or both in the border zone/anesthetic part of the body. Abnormal bursting activity was most pronounced at the posterior inferior aspect of the region of Vc, where stimulation can evoke pain. Therefore this bursting activity may be related to the pain and dysesthesia experienced by the spinal patients.