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Open Access Highly Accessed Research article

Learning alters theta amplitude, theta-gamma coupling and neuronal synchronization in inferotemporal cortex

Keith M Kendrick1, Yang Zhan1, Hanno Fischer1, Alister U Nicol1, Xuejuan Zhang2 and Jianfeng Feng34*

Author affiliations

1 Laboratory of Molecular Signalling, Cognitive and Systems Neuroscience Group, The Babraham Institute, Cambridge CB22 3AT, UK

2 Mathematical Department, Zhejiang Normal University, Zhejiang 321004, PR China

3 Department of Computer Science, Warwick University, Coventry, CV4 7AL, UK

4 Centre for Computational Systems Biology, Fudan University, Shanghai, PR China

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Citation and License

BMC Neuroscience 2011, 12:55  doi:10.1186/1471-2202-12-55

Published: 9 June 2011

Abstract

Background

How 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.

Results

Following 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.

Conclusions

Face 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.