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Abstract

Expectations are generated on multiple timescales. During behavioral planning and working memory utilization, expectations are constructed on the multi-second level (sec), whereas expectations can be externally guided at the sub-second level by rhythmic stimuli (msec). Estimation of multi-second intervals has been associated with monotonic, “climbing” changes in neuron spike rate. On the other hand, sub-second expectations have been associated with rhythmic fluctuations of neuronal excitability in relation to phase of mesoscopic signals. It is not known if changes in gradual spike rate and phase-modulation of neuronal excitability co-occur during multi-second expectations. We studied this question by measuring spike rate, across-trial phase consistency, and phase locked modulations of excitation during a multi-second stimulus expectation task. We recorded single unit spiking and local field potentials from 3 rodent brain regions that have been implicated in time interval estimation, as well as in expectancy and behavioral planning: the prefrontal cortex (PFC), the anterior cingulate cortex (ACC), and the dopamine-producing ventral tegmental area (VTA). A stimulus-evoked phase reset in the PFC, ACC and VTA was observed, which may allow adaptive coding by these neurons and underlie their necessity for behavioral flexibility. In contrast, intrinsic across-trial phase consistency was not observed and phase modulations of excitation did not change in a climbing pattern. These data suggest that expectation over multi-second time intervals is better represented by climbing activity of single dopamine and PFC neurons as compared to mesoscopic signal phase.