Synchronous Oscillatory Neural Ensembles for Rules in the Prefrontal Cortex

Abstract

SUMMARY Intelligent behavior requires acquiring and following rules. Rules define how our behavior should fit different situations. To understand its neural mechanisms, we simultaneously recorded from multiple electrodes in dorsolateral prefrontal cortex (PFC) while monkeys switched between two rules (respond to color versus orientation). We found evidence that oscillatory synchronization of local field potentials (LFPs) formed neural ensembles representing the rules: there were rule-specific increases in synchrony at “beta” (19–40 Hz) frequencies between electrodes. In addition, individual PFC neurons synchronized to the LFP ensemble corresponding to the current rule (color versus orientation). Furthermore, the ensemble encoding the behaviorally dominant orientation rule showed increased “alpha” (6–16 Hz) synchrony when preparing to apply the alternative (weaker) color rule. This suggests that beta-frequency synchrony selects the relevant rule ensemble, while alpha-frequency synchrony deselects a stronger, but currently irrelevant, ensemble. Synchrony may act to dynamically shape task-relevant neural ensembles out of larger, overlapping circuits.

Theta–gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts

“…In our task, the cue signified a color-matching rule ("find the peripheral stimulus matching the color of the cue and enhance its representation against other stimuli"). Correctly interpreting the cue required reactivating neural assemblies coding for the rule representation and applying the rule to the visually available information to eventually prioritize processing of the attended stimulus and filter out uncued stimuli (3,38) (Fig. S8A).…”

“…We thus correlated burst-LFP synchronization of neurons recorded at LFP recording sites that provided theta-phase or gamma-amplitude variations for theta-gamma correlations (SI Result S13). We found that burst synchronization to remote LFP gamma activity varied proportionally with the degree of theta-phase correlation with low-gamma amplitudes (35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47)(48)(49)(50), an effect that was limited to those LFP sites that showed significant theta-gamma correlations (Spearman rank correlation r = 0.2, P = 0.044; Table S2 and SI Result S13). To our knowledge, these findings provide the first quantitative evidence that recording sites with LFP theta phases that engage in longrange gamma correlations also host neurons whose burst firing events synchronize long-range to gamma activity.…”

Bursts of beta oscillation differentiate postperformance activity in the striatum and motor cortex of monkeys performing movement tasks

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Studies of neural oscillations in the beta band (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) have demonstrated modulations in beta-band power associated with sensory and motor events on time scales of 1 s or more, and have shown that these are exaggerated in Parkinson's disease. However, even early reports of beta activity noted extremely fleeting episodes of beta-band oscillation lasting <150 ms. Because the interpretation of possible functions for beta-band oscillations depends strongly on the time scale over which they occur, and because of these oscillations' potential importance in Parkinson's disease and related disorders, we analyzed in detail the distributions of duration and power for beta-band activity in a large dataset recorded in the striatum and motor-premotor cortex of macaque monkeys performing reaching tasks.

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Modafinil Effects on Middle-Frequency Oscillatory Power During Rule Selection in Schizophrenia

“…Furthermore, a recent study of lateral PFC-mediated control processes in monkeys found beta-range oscillations associated with task-relevant rule selection, and alpha oscillations with the unselected rule (Buschman et al, 2012). In humans, beta oscillations are implicated in the control of both movement and cognition by 'endogenous', top-down processes that are usually synonymous with cognitive control (reviewed in Engel and Fries, 2010), and likely mediated via fronto-striatal circuitry (Jenkinson and Brown, 2011).…”

“…Rule selection and representation is a critical element of cognitive control, as it guides taskor context-appropriate responses to the environment (Bunge, 2004). Studies in monkeys have identified how cortical oscillations support rule-representation, including theta (Benchenane et al, 2010;Womelsdorf et al, 2010), alpha and, beta in both rule acquisition (Benchenane et al, 2011) and rule selection (Buschman et al, 2012).…”