Burst and tonic response modes in thalamic neurons during sleep and wakefulness

Citation
Tg. Weyand et al., Burst and tonic response modes in thalamic neurons during sleep and wakefulness, J NEUROPHYS, 85(3), 2001, pp. 1107-1118
Citations number
41
Categorie Soggetti
Neurosciences & Behavoir
Journal title
JOURNAL OF NEUROPHYSIOLOGY
ISSN journal
00223077 → ACNP
Volume
85
Issue
3
Year of publication
2001
Pages
1107 - 1118
Database
ISI
SICI code
0022-3077(200103)85:3<1107:BATRMI>2.0.ZU;2-3
Abstract
Thalamic neurons can exhibit two distinct firing modes: tonic and burst. In the lateral geniculate nucleus (LGN), the tonic mode appears as a relative ly faithful relay of visual information from retina to cortex. The function of the burst mode is less understood. Its prevalence during slow-wave slee p (SWS) and linkage to synchronous cortical electroencephalogram (EEG) sugg est that it has an important role during this form of sleep. Although not n early as common, bursting can also occur during wakefulness. The goal of th is study was to identify conditions that affect burst probability, and to c ompare burst incidence during sleeping and waking. LGN neurons are extraord inarily heterogenous in the degree to which they burst, during both sleepin g and waking. Some LGN neurons never burst under any conditions during wake fulness, and several never burst during slow-wave sleep. During wakefulness , <1% of action potentials were associated with bursting, whereas during sl eep this fraction jumps to 18%. Although bursting was most common during sl ow-wave sleep, more than 50% of the bursting originated from 14% of the LGN cells. Bursting during sleep was largely restricted to episodes lasting 1- 5 s, with <similar to>47% of these episodes being rhythmic and in the delta frequency range (0.5-4 Hz). In wakefulness, although visual stimulation ac counted for the greatest number of bursts, it was still a small fraction of the total response (4%, 742 bursts/17,744 cycles in 93 cells). We identifi ed two variables that appeared to influence burst probability: size of the visual stimuli used to elicit responses and behavioral state. Increased sti mulus size increased burst probability. We attribute this to the increased influence large stimuli have on a cell's inhibitory mechanisms. As with sle ep, a large fraction of bursting originated from a small number of cells. D uring visual stimulation, 50% of bursting was generated by 9% of neurons. I ncreased vigilance was negatively correlated with burst probability. Visual stimuli presented during active fixation (i.e., when the animal must fixat e on an overt fixation point) were less likely to produce bursting, than wh en the same visual stimuli were presented but no fixation point present ("p assive" fixation). Such observations suggest that even brief departures fro m attentive states can hyperpolarize neurons sufficiently to de-inactivate the burst mechanism. Our results provide a new view of the temporal structu re of bursting during slow-wave sleep; one that supports episodic rhythmic activity in the intact animal. In addition, because bursting could be tied to specific conditions within wakefulness, we suggest that bursting has a s pecific function within that state.