Stability of Thalamocortical Synaptic Transmission across Awake Brain States

Abstract

Sensory cortical neurons are highly sensitive to brain state, with many neurons showing changes in spatial and/or temporal response properties and some neurons becoming virtually unresponsive when subjects are not alert. Although some of these changes are undoubtedly attributable to state-related filtering at the thalamic level, another likely source of such effects is the thalamocortical (TC) synapse, where activation of nicotinic receptors on TC terminals have been shown to enhance synaptic transmission in vitro. However, monosynaptic TC synaptic transmission has not been directly examined during different states of alertness. Here, in awake rabbits that shifted between alert and non-alert EEG states, we examined the monosynaptic TC responses and short-term synaptic dynamics generated by spontaneous impulses of single visual and somatosensory TC neurons. We did this using spike-triggered current source-density analysis, an approach that enables assessment of monosynaptic extracellular currents generated in different cortical layers by impulses of single TC afferents. Spontaneous firing rates of TC neurons were higher, and burst rates were much lower in the alert state. However, we found no state-related changes in the amplitude of monosynaptic TC responses when TC spikes with similar preceding interspike interval were compared. Moreover, the relationship between the preceding interspike interval of the TC spike and postsynaptic response amplitude was not influenced by state. These data indicate that TC synaptic transmission and dynamics are highly conserved across different states of alertness and that observed state-related changes in receptive field properties that occur at the cortical level result from other mechanisms.

Effects of cortical activation on sensory responses in barrel cortex

“…Regarding the suppression of low-frequency sensory responses, this has been explained by the increased firing of thalamocortical cells during activation, which leads to the depression of thalamocortical synapses (Boudreau and Ferster 2005;Castro-Alamancos 2004a;Castro-Alamancos and Oldford 2002;Stoelzel et al 2009;Swadlow and Gusev 2001). In addition, depolarization in cortical cells caused by up states has been shown to have complex effects on sensory responses.…”

Control of response reliability by parvalbumin-expressing interneurons in visual cortex

“…LFP traces were band-pass filtered between 1 and 300 Hz 34 , and CSD profiles were computed from the filtered LFP 56,57 . We first converted the 16 recording sites to 18 sites by duplicating the LFP trace of the most superficial site and the deepest site 58,59 . We next smoothed the LFP traces for 16 of the 18 sites (from the 2nd to the 17th site) 58 :…”

“…We first converted the 16 recording sites to 18 sites by duplicating the LFP trace of the most superficial site and the deepest site 58,59 . We next smoothed the LFP traces for 16 of the 18 sites (from the 2nd to the 17th site) 58 :…”

The state of somatosensory cortex during neuromodulation

“…During arousal, vigilance, and paradoxical sleep, cortical networks are typically in a so-called activated or desynchronized state characterized by the absence of slow oscillations (Castro-Alamancos 2009; Moruzzi and Magoun 1949). In sensory cortex, thalamocortical responses driven by sensory signals are very significantly transformed by activated states during arousal (Castro-Alamancos 2002b, 2004a, 2004bCastroAlamancos and Oldford 2002;Hirata and Castro-Alamancos 2011;Stoelzel et al 2009), but the underlying mechanisms of these changes are poorly understood.…”