Sensory coding accuracy and perceptual performance are improved during the desynchronized cortical state

Abstract

Cortical activity changes continuously during the course of the day. At a global scale, population activity varies between the ‘synchronized’ state during sleep and ‘desynchronized’ state during waking. However, whether local fluctuations in population synchrony during wakefulness modulate the accuracy of sensory encoding and behavioral performance is poorly understood. Here, we show that populations of cells in monkey visual cortex exhibit rapid fluctuations in synchrony ranging from desynchronized responses, indicative of high alertness, to highly synchronized responses. These fluctuations are local and control the trial variability in population coding accuracy and behavioral performance in a discrimination task. When local population activity is desynchronized, the correlated variability between neurons is reduced, and network and behavioral performance are enhanced. These findings demonstrate that the structure of variability in local cortical populations is not noise but rather controls how sensory information is optimally integrated with ongoing processes to guide network coding and behavior.

Endogenous activity modulates stimulus and circuit-specific neural tuning and perception

“…However, pre-activation would likely correspond to a higher pre-stimulus response in regions that process a particular stimulus type, not lower as was seen here. Prior studies in early visual cortex in monkeys also showed that lower pre-stimulus activity is associated with 9 improved tuning and behavior (16,17,37). The results of the present study show that these faciliatory effects can be differentially focused in circuits associated with processing specific stimulus types in higher-level visual regions and in regions outside of visual cortex in humans.…”

“…Endogenous activity has rich structure, reflecting the stimulus processing properties of the local neural circuitry(10), broad scale brain network architecture(11), and may reflect statistically optimal representations of the environment(12). Fuctuations in endogenous processes such as arousal(13-15) and alertness (16,17) can influence stimulus processing and behavior. Some theoretical accounts posit that fluctuations of endogenous activity can reflect predictive processes(18) that facilitate stimulus processing in a stimulus-specific manner.…”

The influence of visual cortex on perception is modulated by behavioural state

“…Z-scored pre-trial correlation coefficient on hits: -0.35 ± 0.33, on misses: 0.05 ± 0.18, P = 0.0017 Wilcoxon sign rank test. N = 21 sessions, 14 mice) as recently reported 53,54 . Since cortical synchronicity is linked to perceptual performance, we next asked if the average difference in pre-stimulus synchronicity between hit and miss trials in a given session varies with the level of overall performance in that session.…”

Broadband Dynamics Rather than Frequency-Specific Rhythms Underlie Prediction Error in the Primate Auditory Cortex

“…431Furthermore, the prediction error processing by neural assemblies in the auditory cortex is sustained 432 by an irregular broadband component with small fluctuations lying in a tight range of the non-ergodic 433 dynamical regime h > 1, which has been proposed as an explanation for the 1/f noise of cognitive 434 processes(Grigolini et al, 2009), and large fluctuations with stochastic-like properties. Altogether, 435 this result emphasizes the importance of asynchronous chaotic irregular states for optimal 436 responsiveness to external stimuli(Beaman et al, 2017;Renart et al, 2010; Zerlaut and Destexhe, 437 2017). 438 439 Our findings were enabled by a novel approach to quantify these complex dynamics of neural 440 systems, the so-called brain's "stochastic chaos"(Freeman et al, 2001).…”