Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Theta Rhythms Coordinate Hippocampal—Prefrontal Interactions



PloS Biology

Jones MW, Wilson MA (2005) Theta Rhythms Coordinate Hippocampal–Prefrontal Interactions in a Spatial Memory Task. PLoS Biol 3(12): e402. doi:10.1371/journal.pbio.0030402, November 15, 2005.

Theta Rhythms Coordinate Hippocampal–Prefrontal Interactions in a Spatial Memory Task

Matthew W. Jones1, Matthew A. Wilson1

1 The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, RIKEN-MIT Neuroscience Research Center, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America

The coordinated, rhythmic activity of neuronal populations gives rise to oscillations in local field potentials (LFP) and electroencephalograms at a broad range of frequencies. Throughout the brain, these oscillations potentially constitute clocking mechanisms against which to reference and coordinate the timing of neural firing. Synchronization of these rhythmic activities is likely to reflect or underlie functional interactions between neurons within a defined brain structure, or between disparate populations in distinct structures. Equally, abnormal synchronization may impair functional interactions and contribute to complex cognitive disorders such as schizophrenia and attention deficit/hyperactivity disorder.

Theta rhythms are 4- to 12-Hz oscillations consistently associated with complex behaviors presumed to require mnemonic processing and/or decision-making, for example spatial exploration in rodents, working memory in primates, and navigation and working memory in humans. Dynamic, behavioral modulation of theta rhythms may therefore indicate or mediate cross-neuronal and/or cross-structural interactions during these behaviors. Theta rhythms are found in many mammalian brain structures, but are most prominent in the rodent hippocampus. Here, the firing of individual “place cells”—hippocampal principal excitatory neurons with spatial receptive fields—is coordinated (“phase-locked”) with respect to the local theta rhythm. Thus the action potentials of a given neuron tend to occur during a preferred phase of the theta cycle. This phase-locking of hippocampal spike-timing to ongoing LFP oscillations is an important example of temporal coding in the brain and—in concert with the related phenomenon of phase precession—has been proposed to allow higher-order coding of spatial information than that imparted by the firing-rate pattern alone. It has also been proposed that hippocampal theta rhythms may coordinate neural activity during sensorimotor integration or information encoding.

Neuronal firing phase-locked to the hippocampal theta rhythm has also been described in cingulate cortex, amygdala, entorhinal cortex, striatum, and, most recently, the rat prefrontal cortex. As in the hippocampus, phase-locking in the prefrontal cortex is also accompanied by phase precession. This raises the possibility that phase-locking may play a broader role in defining the temporal relationships between cross-structural activities.

A critical role of working memory is the dynamic and selective incorporation of task-relevant information into decision-making processes. Working memory therefore exemplifies conditions during which multiple disparate brain structures must interact transiently yet coherently. The hub of these interactions is presumed to lie in the prefrontal cortex, whose working-memory functions subserve its broader, integrative roles in establishing context and guiding behavior appropriately. Within the cortex, there is mounting theoretical and electrophysiological evidence from humans and primates suggesting a role for rhythmic activity in working memory.

Our data reveal correlations between behavioral demands and cross-structural neural synchrony: theta-frequency coordination between CA1 and mPFC peaks during behavioral epochs presumed to require effective communication between these two structures. It follows that disruption of such complex cross-structural communication is likely to generate behavioral impairments. For example, schizophrenia is associated with altered GABAergic function in hippocampal and prefrontal interneurons, and is widely presumed to involve disrupted functional connectivity of the prefrontal cortex. Interestingly, schizophrenic patients do show spatial working-memory impairments. The theta-rhythm-mediated coordination of hippocampal–prefrontal activity that we describe here may reflect the nature of cross-structural coordination at network and neuronal levels, and may contribute to both the clinical diagnosis of the impaired interactions likely to underlie cognitive disorders and to characterizing animal models of these diseases



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