Perceptual decisions are based on sensory information but can also be influenced by expectations built from recent experiences. Can the impact of expectations be flexibly modulated based on the outcome of previous decisions? Here, rats perform an auditory task where the probability to repeat the previous stimulus category is varied in trial-blocks. All rats capitalize on these sequence correlations by exploiting a transition bias: a tendency to repeat or alternate their previous response using an internal estimate of the sequence repeating probability. Surprisingly, this bias is null after error trials. The internal estimate however is not reset and it becomes effective again after the next correct response. This behavior is captured by a generative model, whereby a reward-driven modulatory signal gates the impact of the latent model of the environment on the current decision. These results demonstrate that, based on previous outcomes, rats flexibly modulate how expectations influence their decisions.

The spiking activity of cortical neurons is highly variable. This variability is generally correlated among nearby neurons, an effect commonly interpreted to reflect the coactivation of neurons due to anatomically shared inputs. Recent findings, however, indicate that correlations can be dynamically modulated, suggesting that the underlying mechanisms are not well understood. Here, we investigate the hypothesis that correlations are dominated by neuronal coinactivation: the occurrence of brief silent periods during which all neurons in the local network stop firing. We recorded spiking activity from large populations of neurons in the auditory cortex of anesthetized rats across different brain states. During spontaneous activity, the reduction of correlation accompanying brain state desynchronization was largely explained by a decrease in the density of the silent periods. The presentation of a stimulus caused an initial drop of correlations followed by a rebound, a time course that was mimicked by the instantaneous silence density. We built a rate network model with fluctuation-driven transitions between a silent and an active attractor and assumed that neurons fired Poisson spike trains with a rate following the model dynamics. Variations of the network external input altered the transition rate into the silent attractor and reproduced the relation between correlation and silence density found in the data, both in spontaneous and evoked conditions. This suggests that the observed changes in correlation, occurring gradually with brain state variations or abruptly with sensory stimulation, are due to changes in the likeliness of the microcircuit to transiently cease firing.neuronal variability | noise correlations | brain state | auditory cortex | stochastic network dynamics N euronal noise correlations are defined as common fluctuations in the spiking activity of neurons under conditions of constant sensory input or motor output. Traditionally, they have been thought to arise from the dense connectivity of the cortex, such that neighboring neurons sharing a fraction of their inputs should also share a fraction of their output variability (1). Several observations are consistent with this hypothesis: pairwise correlations in the cortex decrease with cell pair distance (2) or with the difference in stimulus selectivity (3), dependencies that could follow from a variation in shared input given the anatomy of cortical circuits. Recent findings, however, challenge this simple interpretation. Recordings in the primate visual cortex have shown that attention or task context can change correlation structure (4-6) and that the magnitude of averaged correlation can be very low (7). In anesthetized rodents correlations decrease with brain state desynchronization (8, 9) or when animals switch from quiet wakefulness to active whisking during waking (10). Moreover, the commonly observed drop of spiking variability following stimulus onset (11-13) seems to occur jointly with a transient decrease in correlation (2, 14, 15). Th...

Standard models of perceptual decision-making postulate that a response is triggered in reaction to stimulus presentation when the accumulated stimulus evidence reaches a decision threshold. This framework excludes however the possibility that informed responses are generated proactively at a time independent of stimulus. Here, we find that, in a free reaction time auditory task in rats, reactive and proactive responses coexist, suggesting that choice selection and motor initiation, commonly viewed as serial processes, are decoupled in general. We capture this behavior by a novel model in which proactive and reactive responses are triggered whenever either of two competing processes, respectively Action Initiation or Evidence Accumulation, reaches a bound. In both types of response, the choice is ultimately informed by the Evidence Accumulation process. The Action Initiation process readily explains premature responses, contributes to urgency effects at long reaction times and mediates the slowing of the responses as animals get satiated and tired during sessions. Moreover, it successfully predicts reaction time distributions when the stimulus was either delayed, advanced or omitted. Overall, these results fundamentally extend standard models of evidence accumulation in decision making by showing that proactive and reactive processes compete for the generation of responses.

Previous research showed that spontaneous neuronal activity presents sloppiness: the collective behavior is strongly determined by a small number of parameter combinations, defined as ‘stiff’ dimensions, while it is insensitive to many others (‘sloppy’ dimensions). Here, we analyzed neural population activity from the auditory cortex of anesthetized rats while the brain spontaneously transited through different synchronized and desynchronized states and intermittently received sensory inputs. We showed that cortical state transitions were determined by changes in stiff parameters associated with the activity of a core of neurons with low responses to stimuli and high centrality within the observed network. In contrast, stimulus-evoked responses evolved along sloppy dimensions associated with the activity of neurons with low centrality and displaying large ongoing and stimulus-evoked fluctuations without affecting the integrity of the network. Our results shed light on the interplay among stability, flexibility, and responsiveness of neuronal collective dynamics during intrinsic and induced activity.

Perceptual decisions are not only determined by current sensory information but are also influenced by expectations based on recent experiences. Can the impact of these expectations be flexibly modulated based on the outcome of previous decisions? We trained rats in several two-alternative forced choice auditory tasks, where the probability to repeat the previous stimulus category was varied in blocks of trials. All rats capitalized on the serial correlations of the stimulus sequence by consistently exploiting a transition bias: a tendency to repeat or alternate their previous response using an internal trial-by-trial estimate of the sequence repeating probability . Surprisingly, this bias was null in trials immediately following an error. The internal estimate however was not reset and it became effective again causing a bias after the next correct response. This ability to rapidly activate and inactivate the bias was captured by a non-linear generative model of rat behavior, whereby a reward-driven modulatory signal gated the use of the latent estimate of the environment statistics on the current decision. These results demonstrate that, based on the outcome of previous choices, rats flexibly modulate how expectations influence their current decisions.

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It is commonly assumed that, during perceptual decisions, the brain integrates stimulus evidence until reaching a decision, and then performs the response. There are conditions, however (e.g. time pressure), in which the initiation of the response must be prepared in anticipation of the stimulus presentation. It is therefore not clear when the timing and the choice of perceptual responses depend exclusively on evidence accumulation, or when preparatory motor signals may interfere with this process. Here, we find that, in a free reaction time auditory discrimination task in rats, the timing of fast responses does not depend on the stimulus, although the choices do, suggesting a decoupling of the mechanisms of action initiation and choice selection. This behavior is captured by a novel model, the Parallel Sensory Integration and Action Model (PSIAM), in which response execution is triggered whenever one of two processes, Action Initiation or Evidence Accumulation, reaches a bound, while choice category is always set by the latter. Based on this separation, the model accurately predicts the distribution of reaction times when the stimulus is omitted, advanced or delayed. Furthermore, we show that changes in Action Initiation mediates both post-error slowing and a gradual slowing of the responses within each session. Overall, these results extend the standard models of perceptual decision-making, and shed a new light on the interaction between action preparation and evidence accumulation.

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