Balanced network dynamics underlie slow autonomous oscillations

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Title Balanced network dynamics underlie slow autonomous oscillations
Publication Type dissertation
School or College School of Medicine
Department Interdepartmental Program in Neuroscience
Author Royzen, Feliks M
Date 2019
Description Numerous synaptic and intrinsic membrane mechanisms have been proposed for generating oscillatory activity in the hippocampus. Few studies, however, have directly measured synaptic conductances and membrane properties during oscillations. The time course and relative contribution of excitatory and inhibitory synaptic conductances, as well as the role of intrinsic membrane properties in amplifying synaptic inputs, remain unclear. To address this issue, we used an isolated whole hippocampal preparation that generates autonomous low-frequency oscillations near the theta range (3-12 Hz). Using 2-photon microscopy and expression of genetically-encoded fluorophores, we obtained on-cell and whole-cell patch recordings of pyramidal cells and fast-firing interneurons in the distal subiculum. Pyramidal cell and interneuron spiking shared similar phase-locking to LFP oscillations. In pyramidal cells, spiking resulted from a concomitant and balanced increase in excitatory and inhibitory synaptic currents. In contrast, interneuron spiking was driven almost exclusively by excitatory synaptic current. Thus, similar to tightly balanced networks underlying hippocampal gamma oscillations and ripples, balanced synaptic inputs in the whole hippocampal preparation drive highly phase-locked spiking at the peak of slower network oscillations. The timescale for hippocampal theta oscillations has been attributed to intrinsic membrane properties that impart resonance and rebound-spiking dynamics to neurons. Autonomous oscillations in the whole hippocampal preparation, which occur near the iv theta frequency band, are generated through a balanced excitation-inhibition mechanism that does not arise from rebound-spiking in pyramidal cells. In order to determine the timescale for autonomous oscillations, we injected pyramidal cells with artificial membrane conductance steps that emulate synaptic input during oscillations in order to evoke low spike rates mimicking those seen in autonomous oscillations. We find that refractory dynamics, particularly those influenced by potassium-channel conductance, inhibit spiking when a second conductance step is applied within 80 ms after the first conductance step. The delay at which spiking and potassium conductances recover matches the timescale of theta (80-320 ms). Thus, the timescale for autonomous oscillations likely arises from an increase in potassium-channel conductance that limits spiking during depolarization, rather than membrane resonance properties that amplify theta frequency inputs.
Type Text
Publisher University of Utah
Dissertation Name Doctor of Philosophy
Language eng
Rights Management (c) Feliks M Royzen
Format application/pdf
Format Medium application/pdf
ARK ark:/87278/s6v93epb
Setname ir_etd
ID 1733652
Reference URL https://collections.lib.utah.edu/ark:/87278/s6v93epb
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