Abstract
Brain activity during wakefulness is characterized by rapid fluctuations in neuronal responses. Whether these fluctuations play any role in modulating the accuracy of behavioral responses is poorly understood. Here, we investigated whether and how trial changes in the population response impact sensory coding in monkey V1 and perceptual performance. Although the responses of individual neurons varied widely across trials, many cells tended to covary with the local population. When population activity was in a 'low' state, neurons had lower evoked responses and correlated variability, yet higher probability to predict perceptual accuracy. The impact of firing rate fluctuations on network and perceptual accuracy was strongest 200 ms before stimulus presentation, and it greatly diminished when the number of cells used to measure the state of the population was decreased. These findings indicate that enhanced perceptual discrimination occurs when population activity is in a 'silent' response mode in which neurons increase information extraction.
Highlights
The dynamics and responsiveness of individual neurons and populations in alert animals vary widely even at short time scales
Our strategy was to quantify the rapid fluctuations in population activity before stimulus presentation, and examine whether these fluctuations help identify optimal network states for signal discrimination task performance
Even though we found a continuum of response states in individual neurons across trials – pre-stimulus firing rates in each session were unimodal rather than reflecting a bimodal distribution (Figure 1E) – our strategy to divide the trials by the median ongoing activity enabled us to compare the network and behavioral performance between two -sized data sets
Summary
The dynamics and responsiveness of individual neurons and populations in alert animals vary widely even at short time scales. Previous investigations using diverse recording techniques – voltage-sensitive dyes (Shoham et al, 1999; Slovin et al, 2002), two-photon calcium imaging (Frye and MacLean, 2016), multi-electrode arrays (Arieli et al, 1995), EEG (Baumgarten et al, 2015; Ergenoglu et al, 2004; Romei et al, 2008; van Dijk et al, 2008), and fMRI (Power et al, 2011; Power et al, 2014; Yeo et al, 2011) – have shown that spontaneous and evoked cortical activity are highly structured in space and time (Ringach, 2009) Consistent with these results, several recent studies have demonstrated that correlated fluctuations in spontaneous and evoked activity can influence stimulus tuning and neural coding (Poulet and Petersen, 2008; Ecker et al, 2014; Tan et al, 2014; McGinley et al, 2015a; Pachitariu et al, 2015; Scholvinck et al, 2015; Niell and Stryker, 2010; Renart et al, 2010). Despite multiple lines of evidence that the dynamics of population activity during wakefulness control how external stimuli are encoded, whether rapid fluctuations in neuronal population activity impact the accuracy of perceptual responses continues to remain poorly understood
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