Role of Field Effects in Coherent Hippocampal Oscillations

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Several brain behavioral, cognitive, or perceptual states are associated with temporally accurate neuronal firing. Understanding the source of this accuracy, which occurs despite significant noise, remain a fundamental problem in brain research. It has been shown that temporal accuracy can be achieved through synchronous synaptic neuronal drive. We note that synchronous neuronal activity also generates extracellular field potentials and that through 'field effect interactions' and these extracellular potentials will coherently polarize a neuronal population. This project proposes and will test two novel mechanisms by which the effect of small electric fields are dramatically amplified at the single neuron level and again at the network level: 1) A small polarization of somatic membrane potential can significantly affect spike timing; 2) A coherent change in spike timing for a large number of neurons can profoundly affect network dynamics and synchronization. We hypothesize that in the hippocampus, endogenous extracellular potentials coherently polarize a neuronal population thereby increasing the accuracy of network spike timing. This project aims to quantify the relationship between naturally occurring 'endogenous' extracellular fields and spike time coherence in neuronal networks. Specifically, small non-uniform fields will be applied to hippocampal slices to quantify the effect of extracellular fields on neuronal membrane potential and spike timing of pyramidal neurons. These results will be integrated into a recurrent network model of spiking neurons to demonstrate the role of field effects in modulating coherent spiking focusing specifically on gamma and theta oscillations. This approach tightly links experimentation with modeling by combining the investigators expertise in electrophysiology and field effects (Bikson), and signal processing/neuronal network modeling (Parra). Our results on small field amplification are equally valid for environmental electric fields (e.g. power lines) and electric fields induced by neuro-prosthetic brain stimulators (e.g. DBS) and thus represent a novel framework for consideration of the effects of low amplitude electric fields. PH: Our brains are exposed to electric fields generated both by the brain itself and by the environment. This project will demonstrate how the brain can 'amplify1 these fields such that electric fields previously considered too small may this be relevant for normal brain function and for disease.