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Synchronous oscillatory neural ensembles for rules in the prefrontal cortex.

ABSTRACT: 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.

SUBMITTER: Buschman TJ

PROVIDER: S-EPMC3907768 | biostudies-literature | 2012 Nov

REPOSITORIES: biostudies-literature

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Synchronous oscillatory neural ensembles for rules in the prefrontal cortex.

Buschman Timothy J TJ Denovellis Eric L EL Diogo Cinira C Bullock Daniel D Miller Earl K EK

Neuron 20121101 4

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 ...[more]

PMID: 23177967

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Project description:The visual system uses two complimentary strategies to process multiple objects simultaneously within a scene and update their spatial positions in real time. It either uses selective attention to individuate a complex, dynamic scene into a few focal objects (i.e., object individuation), or it represents multiple objects as an ensemble by distributing attention more globally across the scene (i.e., ensemble grouping). Neural oscillations may be a key signature for focal object individuation versus distributed ensemble grouping, because they are thought to regulate neural excitability over visual areas through inhibitory control mechanisms. We recorded whole-head MEG data during a multiple-object tracking paradigm, in which human participants (13 female, 11 male) switched between different instructions for object individuation and ensemble grouping on different trials. The stimuli, responses, and the demand to keep track of multiple spatial locations over time were held constant between the two conditions. We observed increased ?-band power (9-13 Hz) packed into oscillatory bursts in bilateral inferior parietal cortex during multiple-object processing. Single-trial analysis revealed greater burst occurrences on object individuation versus ensemble grouping trials. By contrast, we found no differences using standard analyses on across-trials averaged ?-band power. Moreover, the bursting effects occurred only below/at, but not above, the typical capacity limits for multiple-object processing (at ?4 objects). Our findings reveal the real-time neural correlates underlying the dynamic processing of multiple-object scenarios, which are modulated by grouping strategies and capacity. They support a rhythmic, ?-pulsed organization of dynamic attention to multiple objects and ensembles.SIGNIFICANCE STATEMENT Dynamic multiple-object scenarios are an important problem in real-world and computer vision. They require keeping track of multiple objects as they move through space and time. Such problems can be solved in two ways: One can individuate a scene object by object, or alternatively group objects into ensembles. We observed greater occurrences of ?-oscillatory burst events in parietal cortex for processing objects versus ensembles and below/at versus above processing capacity. These results demonstrate a unique top-down mechanism by which the brain dynamically adjusts its computational level between objects and ensembles. They help to explain how the brain copes with its capacity limitations in real-time environments and may lead the way to technological innovations for time-critical video analysis in computer vision.

Dataset Information

Synchronous oscillatory neural ensembles for rules in the prefrontal cortex.

Publications

Synchronous oscillatory neural ensembles for rules in the prefrontal cortex.

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