Abstract
The frontal cortex controls behavioral adaptation in environments governed by complex rules. Many studies have established the relevance of firing rate modulation after informative events signaling whether and how to update the behavioral policy. However, whether the spatiotemporal features of these neuronal activities contribute to encoding imminent behavioral updates remains unclear. We investigated this issue in the dorsal anterior cingulate cortex (dACC) of monkeys while they adapted their behavior based on their memory of feedback from past choices. We analyzed spike trains of both single units and pairs of simultaneously recorded neurons using an algorithm that emulates different biologically plausible decoding circuits. This method permits the assessment of the performance of both spike-count and spike-timing sensitive decoders. In response to the feedback, single neurons emitted stereotypical spike trains whose temporal structure identified informative events with higher accuracy than mere spike count. The optimal decoding time scale was in the range of 70–200 ms, which is significantly shorter than the memory time scale required by the behavioral task. Importantly, the temporal spiking patterns of single units were predictive of the monkeys’ behavioral response time. Furthermore, some features of these spiking patterns often varied between jointly recorded neurons. All together, our results suggest that dACC drives behavioral adaptation through complex spatiotemporal spike coding. They also indicate that downstream networks, which decode dACC feedback signals, are unlikely to act as mere neural integrators.
Highlights
Behavioral adaptation is the process by which animals extract the rules of their environment and learn to respond to cues to increase their chances of survival
We investigated whether summation is relevant during the processing of signals emitted by the dorsal anterior cingulate cortex, a brain area which is thought to control behavioral adaptation in response to feedback cues that indicate the animal’s performance during a task
Our findings suggest that the brain areas processing the signals emitted by the dorsal anterior cingulate cortex are sensitive to spike times and, are unlikely to implement a mere approximate summation of inputs
Summary
Behavioral adaptation is the process by which animals extract the rules of their environment and learn to respond to cues to increase their chances of survival. In the specific case of dACC, a recent theory [1] suggests that this area transmits a graded signal: the expected value of engaging cognitive resources to adapt the behavior. This signal has to be remembered from the moment when the current behavioral policy appears to be improper until the moment when a more appropriate strategy can be implemented. A simple neural integrator [6,7,8,9], which by construction is insensitive to spike timing, would be well suited to decode and memorize this signal This neural integrator could be implemented by the lateral prefrontal cortex [10], which is a plausible dACC target during behavioral adaptation [11]
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