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Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3.

ABSTRACT: Maturation of the cerebral cortex involves the spontaneous emergence of distinct patterns of neuronal synchronization, which regulate neuronal differentiation, synapse formation, and serve as a substrate for information processing. The intrinsic activity patterns that characterize the maturation of cortical layer 2/3 are poorly understood. By using microelectrode array recordings in vivo and in vitro, we show that this development is marked by the emergence of nested - and beta/gamma-oscillations that require NMDA- and GABA(A)-mediated synaptic transmission. The oscillations organized as neuronal avalanches, i.e., they were synchronized across cortical sites forming diverse and millisecond-precise spatiotemporal patterns that distributed in sizes according to a power law with a slope of -1.5. The correspondence between nested oscillations and neuronal avalanches required activation of the dopamine D(1) receptor. We suggest that the repetitive formation of neuronal avalanches provides an intrinsic template for the selective linking of external inputs to developing superficial layers.

SUBMITTER: Gireesh ED

PROVIDER: S-EPMC2396689 | biostudies-literature | 2008 May

REPOSITORIES: biostudies-literature

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Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3.

Gireesh Elakkat D ED Plenz Dietmar D

Proceedings of the National Academy of Sciences of the United States of America 20080522 21

Maturation of the cerebral cortex involves the spontaneous emergence of distinct patterns of neuronal synchronization, which regulate neuronal differentiation, synapse formation, and serve as a substrate for information processing. The intrinsic activity patterns that characterize the maturation of cortical layer 2/3 are poorly understood. By using microelectrode array recordings in vivo and in vitro, we show that this development is marked by the emergence of nested - and beta/gamma-oscillation ...[more]

PMID: 18499802

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Project description:Theta-nested gamma oscillations have been reported in many areas of the brain and are believed to represent a fundamental mechanism to transfer information across spatial and temporal scales. In a series of recent experiments in vitro it has been possible to replicate with an optogenetic theta frequency stimulation several features of cross-frequency coupling (CFC) among theta and gamma rhythms observed in behaving animals. In order to reproduce the main findings of these experiments we have considered a new class of neural mass models able to reproduce exactly the macroscopic dynamics of spiking neural networks. In this framework, we have examined two set-ups able to support collective gamma oscillations: namely, the pyramidal interneuronal network gamma (PING) and the interneuronal network gamma (ING). In both set-ups we observe the emergence of theta-nested gamma oscillations by driving the system with a sinusoidal theta-forcing in proximity of a Hopf bifurcation. These mixed rhythms always display phase amplitude coupling. However, two different types of nested oscillations can be identified: one characterized by a perfect phase locking between theta and gamma rhythms, corresponding to an overall periodic behavior; another one where the locking is imperfect and the dynamics is quasi-periodic or even chaotic. From our analysis it emerges that the locked states are more frequent in the ING set-up. In agreement with the experiments, we find theta-nested gamma oscillations for forcing frequencies in the range [1:10] Hz, whose amplitudes grow proportionally to the forcing intensity and which are clearly modulated by the theta phase. Furthermore, analogously to the experiments, the gamma power and the frequency of the gamma-power peak increase with the forcing amplitude. At variance with experimental findings, the gamma-power peak does not shift to higher frequencies by increasing the theta frequency. This effect can be obtained, in our model, only by incrementing, at the same time, also the stimulation power. An effect achieved by increasing the amplitude either of the noise or of the forcing term proportionally to the theta frequency. On the basis of our analysis both the PING and the ING mechanism give rise to theta-nested gamma oscillations with almost identical features.

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

Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3.

Publications

Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3.

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