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

Abstract

There is a strong correlation between the behavior of an animal and the firing mode (burst or tonic) of thalamic relay neurons. Certain differences between first-and higher-order thalamic relays (which relay peripheral information to the cortex versus information from one cortical area to another, respectively) suggest that more bursting might occur in the higher-order relays. Accordingly, we recorded bursting behavior in single cells from awake, behaving rhesus monkeys in first-order (the lateral geniculate nucleus, the ventral posterior nucleus, and the ventral portion of the medial geniculate nucleus) and higher-order (pulvinar and the medial dorsal nucleus) thalamic relays. We found that the extent of bursting was dramatically greater in the higher-order than in the first-order relays, and this increased bursting correlated with lower spontaneous activity in the higher-order relays. If bursting effectively signals the introduction of new information to a cortical area, as suggested, this increased bursting may be more important in corticocortical transmission than in transmission of primary information to cortex. pulvinar ͉ lateral geniculate nucleus ͉ medial dorsal nucleus ͉ medial geniculate nucleus ͉ ventral posterior nucleus A key feature of the thalamus is the ability of its relay cells to fire in two distinct modes (called tonic and burst), and the firing mode is determined by the inactivation state of voltagegated, T-type Ca 2ϩ channels in the membranes of the soma and dendrites (1-3). This firing mode strongly affects the nature of the signal that is relayed to the cortex (4). For example, compared with tonic mode, burst mode produces much more nonlinear distortion in the relay of information, but the information relayed has greater detectability because of a greater signal-to-noise ratio and stronger activation of postsynaptic cortical targets (4-9). From these properties, the hypothesis has been forwarded that burst firing, with its greater detectability and cortical activation, serves as a ''wake-up call'' to the cortex that there has been a change in the outside world (e.g., a novel stimulus within the receptive field of a relay cell for one of the sensory thalamic nuclei); tonic mode, with its more linear relay of information, is then better suited for a more faithful analysis of the relayed information (4, 7). Thus, burst mode would be more effective for cells dealing with information that is not fully attended to, and the burst would help to redirect attention to the novel stimulus and, ultimately, lead to a shift in firing to tonic mode.Evidence of burst and tonic firing has been reported in various species during waking behavior, including cats (10-12), rats (13-16), 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). However, nearly all of these data were obtained from cells in first-order thalamic relays, namely, the lateral geniculate nu...

Hippocampal atrophy and EEG markers in subjects with mild cognitive impairment

“…Lower alpha frequencies are related to general attention demands. Upper alpha frequencies show a clear relation to higher-order processing demands (Klimesch et al, 1994;Klimesch, 1999;Doppelmays et al, 2002;Ramcharan et al, 2005). So, the increase in the relative alpha2 and alpha3 powers could be due to synchronization in associative cortical areas and/or higher-order thalamic nuclei, where cognitive processes take place.…”

Selective Attenuation of Afferent Synaptic Transmission as a Mechanism of Thalamic Deep Brain Stimulation-Induced Tremor Arrest

“…Although in the awake state the majority of thalamic relay cells are in a tonic firing mode, a small percentage of cells remain in burst mode (Gaze et al, 1964;Lenz et al, 1989). Bursting is particularly prominent in nonlemniscal thalamic neurons (He and Hu, 2002;Ramcharan et al, 2005), in which a more hyperpolarized membrane potential may allow bursts to be triggered through EPSP-LTS coupling (Hu, 2003;Mooney et al, 2004). Therefore, interactions between excitatory synaptic afferents (Pinto et al, 2003;Molnar et al, 2004) and intrinsic membrane currents may play an important role in essential tremor activities.…”

Fewer driver synapses in higher order than in first order thalamic relays

“…There is also evidence for a difference in the postsynaptic effects of cholinergic inputs to thalamic relay cells (Mooney et al, 2004;Varela and Sherman, 2004): in first order nuclei, these are depolarizing, but in higher order nuclei, these are hyperpolarizing for a substantial minority of relay cells. Finally, and perhaps related to the these differences in innervation patterns, recordings from behaving monkeys show that cells in higher order thalamic nuclei tend to be in burst mode much more commonly than are those in first order nuclei (Ramcharan et al, 2005).…”

“…Also, cholinergic inputs from the parabrachial region hyperpolarize many higher order relay cells, whereas these inputs appear to depolarize all first order relay cells (Mooney et al, 2004;Varela and Sherman, 2004). Finally, higher order relay cells exhibit considerably more bursting (Ramcharan et al, 2005), and Li et al (2003a) have described other subtle differences in the temporal response pattern between some first and higher order relay cells.…”