Abstract
The prefrontal cortex and striatum form a recurrent network whose spiking activity encodes multiple types of learning-relevant information. This spike-encoded information is evident in average firing rates, but finer temporal coding might allow multiplexing and enhanced readout across the connected network. We tested this hypothesis in the fronto-striatal network of nonhuman primates during reversal learning of feature values. We found that populations of neurons encoding choice outcomes, outcome prediction errors, and outcome history in their firing rates also carry significant information in their phase-of-firing at a 10–25 Hz band-limited beta frequency at which they synchronize across lateral prefrontal cortex, anterior cingulate cortex and anterior striatum when outcomes were processed. The phase-of-firing code exceeds information that can be obtained from firing rates alone and is evident for inter-areal connections between anterior cingulate cortex, lateral prefrontal cortex and anterior striatum. For the majority of connections, the phase-of-firing information gain is maximal at phases of the beta cycle that were offset from the preferred spiking phase of neurons. Taken together, these findings document enhanced information of three important learning variables at specific phases of firing in the beta cycle at an inter-areally shared beta oscillation frequency during goal-directed behavior.
Highlights
The prefrontal cortex and striatum form a recurrent network whose spiking activity encodes multiple types of learning-relevant information
A large body of evidence has shown that anterior cingulate cortex (ACC) and lateral prefrontal cortex (LPFC) synchronize their local activities at a characteristic beta oscillation frequency[10,11,12,13], and that both areas engage in transient beta rhythmic oscillatory activity with the STR during complex goal-directed tasks[14,15,16,17]
Across all (n = 7938) spike-local field potential (LFP) pairs, we found a pronounced peak of phase synchronization in the beta band (10–25 Hz), with neurons firing on average ~1.15 times more spikes on their preferred, average phase than at the opposite phase when considering the population average in the beta band (Fig. 3b), and ~1.39 times more spikes on the preferred phase when selecting for each neuron the beta frequency with peak synchrony (Supplementary Fig. 3A)
Summary
The prefrontal cortex and striatum form a recurrent network whose spiking activity encodes multiple types of learning-relevant information. The lateral prefrontal cortex (LPFC) and anterior cingulate cortex (ACC) are key brain regions for adjusting to changing environmental task demands[1,2] Both regions project to partly overlapping regions in the anterior striatum (STR), which feeds back projections via the thalamus and thereby close recurrent fronto-striatal-thalamic loops[3]. A large body of evidence has shown that ACC and LPFC synchronize their local activities at a characteristic beta oscillation frequency[10,11,12,13], and that both areas engage in transient beta rhythmic oscillatory activity with the STR during complex goal-directed tasks[14,15,16,17] Whether this beta oscillatory activity is informative for learning and behavioral adjustment has remained unresolved[18,19,20]. These findings document that neural coding of learning variables is enhanced through the phase of firing across the ACC, LPFC, and STR of nonhuman primates
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