Abstract
SummaryThe awake cortex exhibits diverse non-rhythmic network states. However, how these states emerge and how each state impacts network function is unclear. Here, we demonstrate that model networks of spiking neurons with moderate recurrent interactions display a spectrum of non-rhythmic asynchronous dynamics based on the level of afferent excitation, from afferent input-dominated (AD) regimes, characterized by unbalanced synaptic currents and sparse firing, to recurrent input-dominated (RD) regimes, characterized by balanced synaptic currents and dense firing. The model predicted regime-specific relationships between different neural biophysical properties, which were all experimentally validated in the somatosensory cortex (S1) of awake mice. Moreover, AD regimes more precisely encoded spatiotemporal patterns of presynaptic activity, while RD regimes better encoded the strength of afferent inputs. These results provide a theoretical foundation for how recurrent neocortical circuits generate non-rhythmic waking states and how these different states modulate the processing of incoming information.
Highlights
Cortical circuits display spontaneous asynchronous dynamics with low pairwise spiking synchrony (Ecker et al, 2010; Renart et al, 2010)
Is recurrently balanced dynamics a valid model for all the different asynchronous states? If not, do asynchronous dynamics exist beyond the balanced setting? Can we develop a computational model that reveals the mechanisms generating these asynchronous states, that precisely describes the Vm dynamics observed during wakefulness, and that allows us to understand the specific computational advantages of each state?
We reasoned that regimes of intense synaptic activity (Brunel, 2000; Kumar et al, 2008; Renart et al, 2010; van Vreeswijk and Sompolinsky, 1996) should be complemented with regimes of low spiking, where single-neuron dynamics is driven by a few synaptic events, to describe the lower depolarization that characterizes asynchronous regimes associated with moderate arousal (McGinley et al, 2015a)
Summary
Cortical circuits display spontaneous asynchronous dynamics with low pairwise spiking synchrony (Ecker et al, 2010; Renart et al, 2010) Theoretical description of these regimes is based on balanced synaptic activity emerging from recurrent networks (Amit and Brunel, 1997; Destexhe and Contreras, 2006; Hennequin et al, 2017; Kumar et al, 2008; Litwin-Kumar and Doiron, 2012; Parga, 2013; Renart et al, 2010; Tsodyks and Sejnowski, 1995; Vogels et al, 2005; van Vreeswijk and Sompolinsky, 1996). Is recurrently balanced dynamics a valid model for all the different asynchronous states? If not, do asynchronous dynamics exist beyond the balanced setting? Can we develop a computational model that reveals the mechanisms generating these asynchronous states, that precisely describes the Vm dynamics observed during wakefulness, and that allows us to understand the specific computational advantages of each state?
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