Getting Drowsy? Alert/Nonalert Transitions and Visual Thalamocortical Network Dynamics

Abstract

The effects of different EEG brain states on spontaneous firing of cortical populations are not well understood. Such state shifts may occur frequently under natural conditions, and baseline firing patterns can impact neural coding (e.g., signal-to-noise ratios, sparseness of coding). Here, we examine the effects of spontaneous transitions from alert to nonalert awake EEG states in the rabbit visual cortex (5 s before and after the state-shifts). In layer 4, we examined putative spiny neurons and fast-spike GABAergic interneurons; in layer 5, we examined corticotectal neurons. We also examined the behavior of retinotopically aligned dorsal lateral geniculate nucleus (LGNd) neurons, usually recorded simultaneously with the above cortical populations. Despite markedly reduced firing and sharply increased bursting in the LGNd neurons following the transition to the nonalert state, little change occurred in the spiny neurons of layer 4. However, fast-spike neurons of layer 4 showed a paradoxical increase in firing rates as thalamic drive decreased in the nonalert state, even though some of these cells received potent monosynaptic input from the same LGNd neurons whose rates were reduced. The firing rates of corticotectal neurons of layer 5, similarly to spiny cells of layer 4, were not state-dependent, but these cells did become more bursty in the nonalert state, as did the fast-spike cells. These results show that spontaneous firing rates of midlayer spiny populations are remarkably conserved following the shift from alert to nonalert states, despite marked reductions in excitatory thalamic drive and increased activity in local fast-spike inhibitory interneurons.

Directional selective neurons in the awake LGN: response properties and modulation by brain state

“…In awake rabbits, frequent shifts between alert and nonalert brain states are associated with significant changes in spontaneous activity, burst firing (Guido and Weyand 1995;Sherman and Guillery 1996;Weyand et al 2001), and visually driven responses of LGN concentric neurons Cano et al 2006), and some such changes are conveyed to V1 layer 4 simple cells (Bereshpolova et al 2011;Zhuang et al 2014). Our results in LGN DS neurons are consistent with the results for LGN concentric cells, in showing higher spontaneous firing rates, lower burst rates, and stronger responses to visual stimulation in the preferred direction when alert.…”

“…The general surgical procedures have been reported previously (Bereshpolova et al 2007(Bereshpolova et al , 2011Stoelzel et al 2008;Swadlow et al 1998;Zhuang et al 2013) and are briefly described here. All experiments were conducted under the approval of the University of Connecticut Animal Care and Use Committee in accordance with National Institutes of Health Guidelines.…”

“…Multiunit recordings from superficial layers of superior colliculus (SC) were obtained using a threechannel system similar to the LGN system but with low impedance (Ͻ1.5 M⍀) electrodes. Hippocampal EEG and cortical EEG were simultaneously recorded with platinum-iridium microwires for monitoring brain states (Bereshpolova et al 2007(Bereshpolova et al , 2011Bezdudnaya et al 2006;Zhuang et al 2013).…”

“…Notably, this shift in brain state is associated with profound changes in LGN and V1 responses. We have previously shown that LGN concentric cells have higher spontaneous firing rate, lower burst rate, and higher response gain in the alert state than in the nonalert state (Bereshpolova et al 2011;Bezdudnaya et al 2006;Cano et al 2006). Like LGN concentric cells, here we show that DS cells also have significantly higher spontaneous firing rates and lower burst rate in the alert state (mean spontaneous firing rate: alert vs. nonalert: 15.36 Ϯ 1 vs. 9.95 Ϯ 0.95 spikes/s, paired t-test, P Ͻ 0.001, Fig.…”

Hour-long adaptation in the awake early visual system

“…Hippocampal activity in the rabbit can generally be separated into theta activity (4 -8 Hz) and high-voltage, irregular (HVIR) activity. Hippocampal theta activity is associated with cortical desynchronization and an aroused, alert state, whereas HVIR activity is associated with cortical synchronization and a nonaroused, nonalert state (Bereshpolova et al 2011;Green and Arduini 1954;Swadlow and Gusev 2001). During our recordings, rabbits often alternated spontaneously between theta and HVIR activity.…”