Phase of firing coding of learning variables across the fronto-striatal network during feature-based learning

• Published in: Nature communications Vol. 11; no. 1; p. 4669
• Main Authors: Voloh, Benjamin, Oemisch, Mariann, Womelsdorf, Thilo
• Format: Journal Article
• Language: English
• Published: England Nature Publishing Group 16.09.2020; Nature Publishing Group UK; Nature Portfolio
• Subjects: Animals; Cluster Analysis; Coding; Corpus Striatum - cytology; Corpus Striatum - physiology; Cortex (cingulate); Electroencephalography Phase Synchronization; Electrophysiology - methods; Electrophysiology - statistics & numerical data; Firing pattern; Gyrus Cinguli - cytology; Gyrus Cinguli - physiology; Information processing; Learning; Learning - physiology; Macaca mulatta; Male; Multiplexing; Neostriatum; Nerve Net; Neural coding; Neurons; Neurons - physiology; Populations; Prefrontal cortex; Prefrontal Cortex - cytology; Prefrontal Cortex - physiology; Primates; Reversal learning; Reward; Spiking; Temporal cortex; Temporal variations
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-18435-3

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.