Thalamic bursting in rats during different awake behavioral states

Abstract

Thalamic neurons have two firing modes: tonic and bursting. It was originally suggested that bursting occurs only during states such as slow-wave sleep, when little or no information is relayed by the thalamus. However, bursting occurs during wakefulness in the visual and somatosensory thalamus, and could theoretically influence sensory processing. Here we used chronically implanted electrodes to record from the ventroposterior medial thalamic nucleus (VPM) and primary somatosensory cortex (SI) of awake, freely moving rats during different behaviors. These behaviors included quiet immobility, exploratory whisking (large-amplitude whisker movements), and whisker twitching (small-amplitude, 7-to 12-Hz whisker movements). We demonstrated that thalamic bursting appeared during the oscillatory activity occurring before whisker twitching movements, and continued throughout the whisker twitching. Further, thalamic bursting occurred during whisker twitching substantially more often than during the other behaviors, and a neuron was most likely to respond to a stimulus if a burst occurred Ϸ120 ms before the stimulation. In addition, the amount of cortical area activated was similar to that during whisking. However, when SI was inactivated by muscimol infusion, whisker twitching was never observed. Finally, we used a statistical technique called partial directed coherence to identify the direction of influence of neural activity between VPM and SI, and observed that there was more directional coherence from SI to VPM during whisker twitching than during the other behaviors. Based on these findings, we propose that during whisker twitching, a descending signal from SI triggers thalamic bursting that primes the thalamocortical loop for enhanced signal detection during the whisker twitching behavior. I t has been demonstrated that thalamic relay neurons have two distinct modes of firing. These are the tonic firing mode, in which neurons fire single action potentials, and the bursting mode, in which cells fire bursts of two to seven action potentials (1, 2). During the tonic firing mode, cells respond to stimuli with individual spikes that can closely follow incoming activity (3-5). In contrast, during the burst mode, cells respond to incoming stimuli with bursts that do not directly resemble the afferent activity because the bursts are all-or-nothing events, and there is a long refractory period between bursts (4, 5).It was originally thought that the tonic mode was associated with behavioral states, such as wakefulness and sleep, during which afferent stimuli are readily relayed by the thalamus (3, 6-8). In contrast, the bursting mode was thought to occur only during times when no afferent information was, in theory, transmitted by the thalamus (refs. 1, 9, and 10; see ref. 11 for review), such as during slow-wave sleep, barbiturate anesthesia, and pathological conditions such as seizure activity. However, it has recently been demonstrated that thalamic bursting can occur during awake states as well, in multiple species (12-...

Cortical control of adaptation and sensory relay mode in the thalamus

“…However, the coexistence of burst and tonic sensory responses reported here is in line with other studies in anesthetized and awake animals which demonstrate that sensory information is encoded through both tonic and burst spikes (10,37). Furthermore, bursts have been shown to be part of the sensory response during active tasks (8,11,16), and bursts are systematically related to the sensory input (Fig. 2); this relationship would not be expected if sensory relay is suppressed by bursts (38).…”

“…In burst mode, sensory inputs are relayed as short, rapid clusters of APs; in contrast, in tonic mode the same inputs are translated into single APs. Both tonic and burst modes have been described during anesthesia/sleep and wakefulness/behavior, with a pronounced shift toward the tonic mode during alertness (8)(9)(10)(11)(12).…”

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

“…However, recent evidence suggests that thalamic bursting plays a fundamental role in sensory processing (53,54). Studies of visual (55) and somatosensory (30,53) pathways demonstrate the presence of thalamic bursting in awake and attentive states, implying that bursting activity modulates sensory perception. Intermittent activation of multiple long-range circuits to integrate major sensory cortices suggests that multisensory integration is essential to shape sensory perceptions that could not otherwise be achieved with only one sense (56,57).…”

“…Thalamo-cortical circuits, particularly the somatosensory thalamo-cortical circuits in rodents, are excellent models of longrange projections often studied for their straightforward circuit architecture with monosynaptic excitatory cortical input (25,26). In addition, the thalamus can control cortical states (27-29) and modulate spontaneous cortical activity based on different cortical states (30,31). These studies suggest that the thalamo-corticothalamic networks are integral to facilitating diverse functional neural integration across the entire brain.…”

Higher-order thalamic relays burst more than first-order relays

“…Evidence of burst and tonic firing has been reported in various species during waking behavior, including cats (10)(11)(12), rats (13)(14)(15)(16), guinea pigs (17,18), rabbits (5,6), monkeys (19), and humans (20)(21)(22). In general, bursting is relatively rare during full wakefulness and more common during periods of inattention or drowsiness (6).…”