Response outcome gates the effect of spontaneous cortical state fluctuations on perceptual decisions

Abstract

Sensory responses of cortical neurons are more discriminable when evoked on a baseline of desynchronized spontaneous activity, but cortical desynchronization has not generally been associated with more accurate perceptual decisions. Here we show that mice perform more accurate auditory judgements when activity in the auditory cortex is elevated and desynchronized before stimulus onset, but only if the previous trial was an error, and that this relationship is occluded if previous outcome is ignored. We confirmed that the outcome-dependent effect of brain state on performance is neither due to idiosyncratic associations between the slow components of either signal, nor to the existence of specific cortical states evident only after errors. Instead, errors appear to gate the effect of cortical state fluctuations on discrimination accuracy. Neither facial movements nor pupil size during the baseline were associated with accuracy, but they were predictive of measures of responsivity, such as the probability of not responding to the stimulus or of responding prematurely. These results suggest that the functional role of cortical state on behavior is dynamic and constantly regulated by performance monitoring systems.

Episodic recruitment of attractor dynamics in frontal cortex reveals distinct mechanisms for forgetting and lack of cognitive control in short-term memory

“…S13; n = 31 sessions; Methods). Thus, the RepL phase tended to coincide with epochs of elevated synchronous, oscillatory spiking in ALM, an activity pattern commonly observed in cortical recordings in head-fixed behaving mice (Jacobs et al 2020; Reato et al 2023).…”

“…Lastly, we turned to investigate whether the switching between STM and RepL phases correlated with changes in network synchrony, a metric commonly used to monitor changes in brain state (Jacobs et al 2020; Einstein et al 2017; McGinley et al 2015; Reato et al 2023). As reported previously (Jacobs et al 2020; Reato et al 2023), synchronized spiking activity across the recorded neurons was sporadically but clearly observed in some trials (Fig. 6a).…”

“…Another study carrying out a visual two-alternative choice task, found a specific impact on engagement (higher synchrony causing more misses) but not on perceptual discriminability (Jacobs et al 2020). More recently, Reato and colleagues have found that elevated cortical synchrony can reduce discrimination performance in a two-alternative forced-choice auditory task but only if the previous outcome was an error (Reato et al 2023). The authors explain the absence of impact of synchronous activity by arguing that “when discriminating simple sensory stimuli, mice can operate in a behavioral state equivalent to ‘flow’ during streaks of correct trials”.…”

“…We fitted a GLMM to quantify the influence that the different task variables had on the choices of each individual mouse (Busse et al 2011; Frund, Wichmann, and Macke 2014; Abrahamyan et al 2016; Braun, Urai, and Donner 2018; Hermoso-Mendizabal et al 2020; Reato et al 2023). We used both mouse Groups #1 and #2 together in this analysis.…”

Facial expressions in mice reveal latent cognitive variables and their neural correlates

“…To make the best case for the link between internal state and bodily expressions, rich behavioral observations using high-resolution video recordings during task execution can be combined with large-scale neural recordings, as pioneered by recent work in mice and non-human primates (15)(16)(17)(18)(19)(20). These studies have shown that incidental movements can account for a larger fraction of the variance of neural activity than task-related movements (but see (20)), and are informative about the internal state of engagement (see also (21)), and that the extent to which incidental movements shape neural activity depends on the brain area (18,20).…”