State-related modulation of thalamic somatosensory responses in the awake monkey

Abstract

1. These experiments were performed to assess the nature and extent of the modulation of somatosensory transmission through the thalamus of the awake primate brain. We investigated physiologically induced modulation occurring during changes in state of arousal within the waking state. Changes in thalamic responsiveness during the sleep-waking cycle were not studied. 2. We recorded from single units in several nuclei within the ventral posterior region of the thalamus (VP) of awake squirrel monkeys (Saimiri sciureus). Recording sites included the ventral posterior lateral, ventral posterior medial, ventral posterior inferior, ventral lateral, and thalamic reticular nuclei. Four hundred twenty-seven thalamic units were tested for responsiveness to innocuous and noxious somatic stimulation of cutaneous (hair and skin) and deep (muscle and tendon) structures and to innocuous electrical stimulation of the spinal lemniscus (SL). Noxious stimuli were just sufficient to evoke withdrawal and did not cause tissue damage. 3. All neurons were spontaneously active in the absence of intentional stimulation. Only 260 (60.9%) of the neurons recorded in VP responded to somatic or SL stimulation. Based on their responsiveness to somatic stimuli, we classified neurons as cutaneous (67.7% or 176/260) if responsive to hair and/or skin stimulation or as deep (18.8% or 49/260) if responsive only to manipulation of joints or palpation of muscles or tendons. Thirty-five other cells (13.5%) responded best to brisk innocuous taps applied to the somatic receptive field and were placed in a separate group. Cutaneous units were subclassified as low-threshold (LT, 86.9% or 153/176) if responding maximally to innocuous stimuli only or as wide dynamic range (WDR, 13.1% or 23/176) if responding preferentially to noxious stimuli. No neurons responded exclusively to noxious stimuli. Single-pulse SL stimulation evoked discharges at an average latency of 3.3 +/- 4.8 (SD) ms in 51/132 (38.6%) LT neurons tested and similarly affected 7 of 12 WDR cells tested at an average latency of 1.54 +/- 0.39 ms. 4. We tested 88 neurons for changes in activity as the monkey's state of arousal shifted between quiet waking (QW), waking movement (WM), and drowsy (D) states as defined by behavioral and electroencephalographic criteria. The responses of 42% of the 88 somatically activated cells tested (n = 37) showed arousal-related response modulation (ARM). ARM produced a mean change in evoked activity of 40.1% (+/- 23.5 SD) relative to that cell's maximal response and the specific state of arousal during which the maximal response occurred. Neurons classified as WDR were equally likely to exhibit ARM as LT neurons.(ABSTRACT TRUNCATED AT 400 WORDS)