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

Abstract

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.

More than spikes: common oscillatory mechanisms for content specific neural representations during perception and memory

“…Thus, single neuron firing and gamma are largest and convey the most content-specific information at particular frequencies and phases, suggesting that assemblies are organized by the frequency and phase of low-frequency oscillations [47,51]. Given that single-unit phase-locking [33] and PAC [52-54] are strongly associated with learning, they may also serve to transform sensory representations into frequency and phase-coded engrams.…”

Cross-frequency coupling in real and virtual brain networks

“…Recently, more and more evidence suggests that corresponding CFC between these frequency bands plays a crucial role in this and other processes, e.g., neuronal computation, communication, and learning (Schack et al, 2002; Schack and Weiss, 2005; Canolty et al, 2006; Jensen and Colgin, 2007; Cohen, 2008; Tort et al, 2008, 2009; Doesburg et al, 2009; Canolty and Knight, 2010; Kendrick et al, 2011). In the study of Schack et al (2002), increased power in the theta and the gamma frequency bands was accompanied by strong phase coupling by means of cross- BIC between theta frequency at Fz and gamma frequency at F3 and Fp1, respectively, for memorizing number words.…”

Chronic stimulation of cultured neuronal networks boosts low-frequency oscillatory activity at theta and gamma with spikes phase-locked to gamma frequencies

“…Although theta waves have been associated with both inhibitory and excitatory connections (Kendrick et al 2011), our observed increased ratio of excitatory to inhibitory composition with chronic stimulation suggests that less inhibitory drive contributes to the increased theta power.…”