Neocortical inhibitory activities and long-range afferents contribute to the synchronous onset of silent states of the neocortical slow oscillation

Abstract

Lemieux M, Chauvette S, Timofeev I. Neocortical inhibitory activities and long-range afferents contribute to the synchronous onset of silent states of the neocortical slow oscillation. J Neurophysiol 113: 768-779, 2015. First published November 12, 2014 doi:10.1152/jn.00858.2013.-During slowwave sleep, neurons of the thalamocortical network are engaged in a slow oscillation (Ͻ1 Hz), which consists of an alternation between the active and the silent states. Several studies have provided insights on the transition from the silent, which are essentially periods of disfacilitation, to the active states. However, the conditions leading to the synchronous onset of the silent state remain elusive. We hypothesized that a synchronous input to local inhibitory neurons could contribute to the transition to the silent state in the cat suprasylvian gyrus during natural sleep and under ketamine-xylazine anesthesia. After partial and complete deafferentation of the cortex, we found that the silent state onset was more variable among remote sites. We found that the transition to the silent state was preceded by a reduction in excitatory postsynaptic potentials and firing probability in cortical neurons. We tested the impact of chloride-mediated inhibition in the silent-state onset. We uncovered a long-duration (100 -300 ms) inhibitory barrage occurring about 250 ms before the silent state onset in 3-6% of neurons during anesthesia and in 12-15% of cases during natural sleep. These inhibitory activities caused a decrease in cortical firing that reduced the excitatory drive in the neocortical network. That chain reaction of disfacilitation ends up on the silent state. Electrical stimuli could trigger a network silent state with a maximal efficacy in deep cortical layers. We conclude that long-range afferents to the neocortex and chloride-mediated inhibition play a role in the initiation of the silent state. slow oscillation; long-range afferents; chloride-mediated inhibition; intracellular recordings SLOW OSCILLATION IS THE HALLMARK of the slow-wave sleep but also of several anesthetics, including ketamine-xylazine (Contreras and Steriade 1995; Steriade et al.

Neocortical Focus

“…Our current study (Lemieux, Chauvette, & Timofeev, 2014) indicates that thalamus may be such a structure. Our current study (Lemieux, Chauvette, & Timofeev, 2014) indicates that thalamus may be such a structure.…”

“…After a chronic blockade of activity, Na + currents increase and K + currents decrease in size, resulting in an enhanced responsiveness of pyramidal cells to current injection (Desai, Rutherford, & Turrigiano, 1999). However, after 15-20 h, homeostatic upregulation of excitability was able to recover the slow oscillation (Lemieux, Chauvette, et al, 2014). Thus, homeostatic plasticity controls the levels of neuronal activity through synaptic and intrinsic mechanisms (Murthy et al, 2001;Turrigiano et al, 1998).…”

Moderate Cortical Cooling Eliminates Thalamocortical Silent States during Slow Oscillation

“…A similar decrease in temperature has been found to reduce the vesicle release probability within synapses, increase latency, or lead to asynchronous release of neurotransmitters (Katz and Miledi, 1965;Jasper et al, 1970;Hardingham and Larkman, 1998;Volgushev et al, 2004;Yang et al, 2005). Only deep cooling, below 10°C, completely silenced the network with a depolarizing block of sodium channels and abolished synaptic release (Jasper et al, 1970;Volgushev et al, 2000). We hypothesized that mild/moderate cooling (heating) of the cortex can be used as a fast and reversible tool to manipulate network activities via its bidirectional effects on intrinsic neuronal excitability and synaptic release properties.…”

“…During REM sleep and the waking state, thalamocortical neurons are depolarized (Hirsch et al, 1983;Woody et al, 2003). There are at least two main causes for such a depolarization.…”

“…In these conditions, the cortical network activity switches to persistent active states (Timofeev et al, 2000;Steriade et al, 2001). In modeling studies, the light increase in the resting membrane potential evoked by the partial blocking of potassium leakage channels was sufficient to transform thalamocortical slow-wave activity into wake-like persistent activity Compte et al, 2003;Hill and Tononi, 2005). At the level of synapses, acetylcholine reduces the release probability in the cortex and reduces short-term synaptic depression (Gil et al, 1997;Hasselmo and McGaughy, 2004;Eggermann and Feldmeyer, 2009;.…”