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

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Kendrick, Keith M., Zhan, Yang, Fischer, Hanno, Nicol, Alister U., Zhang, Xuejuan and Feng, Jianfeng. (2011) Learning alters theta amplitude, theta-gamma coupling and neuronal synchronization in inferotemporal cortex. BMC Neuroscience, Vol.12 (No.55). ISSN 1471-2202

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Official URL: http://dx.doi.org/10.1186/1471-2202-12-55

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.

Item Type:	Journal Article
Subjects:	Q Science > QP Physiology
Divisions:	Faculty of Science > Computer Science
Library of Congress Subject Headings (LCSH):	Learning -- Physiological aspects, Neural networks (Neurobiology), Theta rhythm
Journal or Publication Title:	BMC Neuroscience
Publisher:	BioMed Central Ltd.
ISSN:	1471-2202
Date:	9 June 2011
Volume:	Vol.12
Number:	No.55
Identification Number:	10.1186/1471-2202-12-55
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Engineering and Physical Sciences Research Council (EPSRC), Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), SEARCH Foundation, European Union (EU), Guo jia zi ran ke xue ji jin wei yuan hui (China) [National Natural Science Foundation of China] (NSFC)
Grant number:	BBS/B/07691 (BBSRC), 10771155 (NSFC), 10971196 (NSFC)
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URI:	http://wrap.warwick.ac.uk/id/eprint/35928