Burst and tonic firing in thalamic cells of unanesthetized, 
behaving monkeys

Ramcharan, Eion J.; Gnadt, James W.; Sherman, S. Murray

doi:10.1017/s0952523800171056

Cited by 180 publications

(166 citation statements)

References 37 publications

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“…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).…”

Section: Discussionsupporting

confidence: 92%

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Cortical control of adaptation and sensory relay mode in the thalamus

Mease

Krieger

Groh

2014

Proc. Natl. Acad. Sci. U.S.A.

116

183

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A major synaptic input to the thalamus originates from neurons in cortical layer 6 (L6); however, the function of this cortico-thalamic pathway during sensory processing is not well understood. In the mouse whisker system, we found that optogenetic stimulation of L6 in vivo results in a mixture of hyperpolarization and depolarization in the thalamic target neurons. The hyperpolarization was transient, and for longer L6 activation (>200 ms), thalamic neurons reached a depolarized resting membrane potential which affected key features of thalamic sensory processing. Most importantly, L6 stimulation reduced the adaptation of thalamic responses to repetitive whisker stimulation, thereby allowing thalamic neurons to relay higher frequencies of sensory input. Furthermore, L6 controlled the thalamic response mode by shifting thalamo-cortical transmission from bursting to single spiking. Analysis of intracellular sensory responses suggests that L6 impacts these thalamic properties by controlling the resting membrane potential and the availability of the transient calcium current I T , a hallmark of thalamic excitability. In summary, L6 input to the thalamus can shape both the overall gain and the temporal dynamics of sensory responses that reach the cortex. S ensory signals en route to the cortex undergo profound signal transformations in the thalamus. One important thalamic transformation is sensory adaptation. Adaptation is a common characteristic of sensory systems in which neural output adjusts to the statistics and dynamics of past stimuli, thereby better encoding small stimulus changes across a wide range of scales despite the limited range of possible neural outputs (1-3). Thalamic sensory adaptation is characterized by a steep decrease in action potential (AP) activity during sustained sensory stimulation (4-7), decreasing the efficacy at which subsequent sensory stimuli are transmitted to the cortex.The widely reported duality of thalamic response mode is another key property of thalamic information processing which further affects how sensory input reaches the cortex. 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 (8-12).Although the exact information content of thalamic bursts is not yet clear, it has been suggested that bursting may signal novel stimuli to the cortex, whereas the tonic mode enables linear encoding of fine stimulus details, e.g., when an object is examined (13,14). One issue hampering the interpretation of burst/ tonic responses is that currently it is unknown if the cortex itself is involved in the rapid changes in firing modes seen in the awake and anesthetized animal (15, 16) and which mechanisms initiate these shifts in vivo.On the biophysical level, the response mode depends on the resting membrane potential (RMP), which controls...

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Section: Discussionsupporting

confidence: 92%

“…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).…”

mentioning

confidence: 99%

Cortical control of adaptation and sensory relay mode in the thalamus

Mease

Krieger

Groh

2014

Proc. Natl. Acad. Sci. U.S.A.

116

183

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“…11 and 38; for review see ref., 39) and in vivo (1,40). These results corroborate other studies that have shown bursting activity during wakefulness in cats (13,14), guinea pigs (15), rabbits (16), and monkeys (17,18). Thus, it is clear that bursting can occur during wakefulness and, indeed, can be observed during periods of sensory processing (12)(13)(14).…”

Section: The Burst Firing Mode Is Not Limited To Sleep and Pathologicsupporting

confidence: 87%

“…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)(13)(14)(15)(16)(17)(18), and that sensory information can be conveyed to the cortex during the burst activity (16).…”

mentioning

confidence: 99%

Thalamic bursting in rats during different awake behavioral states

Fanselow

Sameshima²,

Baccalá³

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

218

174

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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-...

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“…If visual TRN neurons project back to the LGN neurons from which they receive their inputs (to the neurons representing the same part of the visual field), they would form "closed loop" connections, resulting in feedback inhibition. It has been suggested that during wakefulness, feedback inhibition initiates a rhythmic burst firing in LGN relay neurons, which may serve to alert visual cortex of behaviorally relevant sensory input (Crick, 1984;Sherman and Guillery, 1996) and facilitate signal transmission during visual target acquisition and early phases of fixation (Guido and Weyand, 1995; also see Ramcharan et al, 2000). The predominant increase in visual TRN activity that we have shown would be consistent with this view, because this increase in activity would be passed to the LGN as an increase in inhibition, resulting in the hyperpolarization of the LGN membrane and the consequent switching of these visual thalamic relay neurons from tonic to burst mode (Llinas and Jahnsen, 1982;Jahnsen and Llinas, 1984a,b;Sherman and Koch, 1986).…”

Section: Trn Modulation With Attentionmentioning

confidence: 99%

Attentional Modulation of Thalamic Reticular Neurons

McAlonan

Cavanaugh²,

Wurtz³

2006

J. Neurosci.

207

156

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The major pathway for visual information reaching cerebral cortex is through the lateral geniculate nucleus (LGN) of the thalamus. Acting on this vital relay is another thalamic nucleus, the thalamic reticular nucleus (TRN). This nucleus receives topographically organized collaterals from both thalamus and cortex and sends similarly organized projections back to thalamus. The inputs to the TRN are excitatory, but the output back to the thalamic relay is inhibitory, providing an ideal organization for modulating visual activity during early processing. This functional architecture led Crick in 1984 to hypothesize that TRN serves to direct a searchlight of attention to different regions of the topographic map; however, despite the substantial influence of this hypothesis, the activity of TRN neurons has never been determined during an attention task. We have determined the nature of the response of visual TRN neurons in awake monkeys, and the modulation of that response as the monkeys shifted attention between visual and auditory stimuli. Visual TRN neurons had a strong (194 spikes/s) and fast (25 ms latency) transient increase of activity to spots of light falling in their receptive fields, as well as high background firing rate (45 spikes/s). When attention shifted to the spots of light, the amplitude of the transient visual response typically increased, whereas other neuronal response characteristics remained unchanged. Thus, as predicted previously, TRN activity is modified by shifts of visual attention, and these attentional changes could influence visual processing in LGN via the inhibitory connections back to the thalamus.

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Burst and tonic firing in thalamic cells of unanesthetized, behaving monkeys

Cited by 180 publications

References 37 publications

Cortical control of adaptation and sensory relay mode in the thalamus

Cortical control of adaptation and sensory relay mode in the thalamus

Thalamic bursting in rats during different awake behavioral states

Attentional Modulation of Thalamic Reticular Neurons

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