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Theta-gamma coupling increases during the learning of item-context associations.

ABSTRACT: Phase-amplitude cross-frequency coupling (CFC) between theta (4-12 Hz) and gamma (30-100 Hz) oscillations occurs frequently in the hippocampus. However, it still remains unclear whether theta-gamma coupling has any functional significance. To address this issue, we studied CFC in local field potential oscillations recorded from the CA3 region of the dorsal hippocampus of rats as they learned to associate items with their spatial context. During the course of learning, the amplitude of the low gamma subband (30-60 Hz) became more strongly modulated by theta phase in CA3, and higher levels of theta-gamma modulation were maintained throughout overtraining sessions. Furthermore, the strength of theta-gamma coupling was directly correlated with the increase in performance accuracy during learning sessions. These findings suggest a role for hippocampal theta-gamma coupling in memory recall.

SUBMITTER: Tort AB

PROVIDER: S-EPMC2791641 | biostudies-literature | 2009 Dec

REPOSITORIES: biostudies-literature

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Theta-gamma coupling increases during the learning of item-context associations.

Tort Adriano B L AB Komorowski Robert W RW Manns Joseph R JR Kopell Nancy J NJ Eichenbaum Howard H

Proceedings of the National Academy of Sciences of the United States of America 20091123 49

Phase-amplitude cross-frequency coupling (CFC) between theta (4-12 Hz) and gamma (30-100 Hz) oscillations occurs frequently in the hippocampus. However, it still remains unclear whether theta-gamma coupling has any functional significance. To address this issue, we studied CFC in local field potential oscillations recorded from the CA3 region of the dorsal hippocampus of rats as they learned to associate items with their spatial context. During the course of learning, the amplitude of the low ga ...[more]

PMID: 19934062

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Project description:BackgroundHow oscillatory brain rhythms alone, or in combination, influence cortical information processing to support learning has yet to be fully established. Local field potential and multi-unit neuronal activity recordings were made from 64-electrode arrays in the inferotemporal cortex of conscious sheep during and after visual discrimination learning of face or object pairs. A neural network model has been developed to simulate and aid functional interpretation of learning-evoked changes.ResultsFollowing learning the amplitude of theta (4-8 Hz), but not gamma (30-70 Hz) oscillations was increased, as was the ratio of theta to gamma. Over 75% of electrodes showed significant coupling between theta phase and gamma amplitude (theta-nested gamma). The strength of this coupling was also increased following learning and this was not simply a consequence of increased theta amplitude. Actual discrimination performance was significantly correlated with theta and theta-gamma coupling changes. Neuronal activity was phase-locked with theta but learning had no effect on firing rates or the magnitude or latencies of visual evoked potentials during stimuli. The neural network model developed showed that a combination of fast and slow inhibitory interneurons could generate theta-nested gamma. By increasing N-methyl-D-aspartate receptor sensitivity in the model similar changes were produced as in inferotemporal cortex after learning. The model showed that these changes could potentiate the firing of downstream neurons by a temporal desynchronization of excitatory neuron output without increasing the firing frequencies of the latter. This desynchronization effect was confirmed in IT neuronal activity following learning and its magnitude was correlated with discrimination performance.ConclusionsFace discrimination learning produces significant increases in both theta amplitude and the strength of theta-gamma coupling in the inferotemporal cortex which are correlated with behavioral performance. A network model which can reproduce these changes suggests that a key function of such learning-evoked alterations in theta and theta-nested gamma activity may be increased temporal desynchronization in neuronal firing leading to optimal timing of inputs to downstream neural networks potentiating their responses. In this way learning can produce potentiation in neural networks simply through altering the temporal pattern of their inputs.

Dataset Information

Theta-gamma coupling increases during the learning of item-context associations.

Publications

Theta-gamma coupling increases during the learning of item-context associations.

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