Suppression of cortical neural variability is stimulus- and state-dependent

Abstract

Internally generated, spontaneous activity is ubiquitous in the cortex, yet it does not appear to have a significant negative impact on sensory processing. Various studies have found that stimulus onset reduces the variability of cortical responses, but the characteristics of this suppression remained unexplored. By recording multiunit activity from awake and anesthetized rats, we investigated whether and how this noise suppression depends on properties of the stimulus and on the state of the cortex. In agreement with theoretical predictions, we found that the degree of noise suppression in awake rats has a nonmonotonic dependence on the temporal frequency of a flickering visual stimulus with an optimal frequency for noise suppression ~2 Hz. This effect cannot be explained by features of the power spectrum of the spontaneous neural activity. The nonmonotonic frequency dependence of the suppression of variability gradually disappears under increasing levels of anesthesia and shifts to a monotonic pattern of increasing suppression with decreasing frequency. Signal-to-noise ratios show a similar, although inverted, dependence on cortical state and frequency. These results suggest the existence of an active noise suppression mechanism in the awake cortical system that is tuned to support signal propagation and coding.

Patterns of Modulation in the Activity and Connectivity of Motor Cortex during the Repeated Generation of Movement Sequences

“…These results are in agreement with recent reports (He, 2013) of a reduction in variability in the fMRI BOLD signals following stimulus onset, as well as with animal studies that showed that intrinsically generated spontaneous fluctuations in neuronal activity undergo suppression during task-evoked activity throughout the cortex in a broad range of conditions (White, Abbott, & Fiser, 2012;Churchland et al, 2010;Churchland, Yu, Ryu, Santhanam, & Shenoy, 2006). The decline in variability implies that cortical circuits can be stabilized by an input or a task and may support information encoding (He, 2013;White et al, 2012;Churchland et al, 2010). In the current study, however, the large decreases in the M1 signal variability with task performance were not differentially modulated by the level of experience with the specific movement sequence or by its repetition across the brief rest interval.…”

Spontaneous and Task-Evoked Brain Activity Negatively Interact

“…Variability reduction following stimulus onset was previously reported in neuronal firing (Werner and Mountcastle, 1963; Churchland et al, 2010; Chang et al, 2012; White et al, 2012). However, given the complex relationships between the fMRI signal, neuronal firing and local field potentials (LFP) and the dissociation between the fMRI signal and neuronal firing under various conditions (e.g., Logothetis, 2008; Maier et al, 2008; He and Raichle, 2009), our finding of variability reduction in the fMRI signal does not follow trivially from this previous work.…”

A spontaneous state of weakly correlated synaptic excitation and inhibition in visual cortex

“…Finally, we note that the variability of membrane potential, synaptic excitation and inhibition also depends on sensory stimulus and cortical area (Heil, 1997; Stiebler et al, 1997; DeWeese et al, 2003; Monier et al, 2003; Tan et al, 2004, 2007; Finn et al, 2007; Gutnisky and Dragoi, 2008; Herikstad et al, 2011; Hansen et al, 2012; White et al, 2012). The covariability of excitation and inhibition should therefore also be measured for different sensory stimuli in different cortical areas.…”