Date of Award

Summer 8-15-2015

Author's School

Graduate School of Arts and Sciences

Author's Department

Biology & Biomedical Sciences (Neurosciences)

Degree Name

Doctor of Philosophy (PhD)

Degree Type

Dissertation

Abstract

Encoding information into the timing patterns of action potentials, or spikes, is a strategy used broadly in neural circuits. This type of coding scheme requires downstream neurons to be sensitive to the temporal patterns of presynaptic inputs. Indeed, neurons with temporal filtering properties have been found in a wide range of sensory pathways. However, how such response properties arise was previously not well understood. The goal of my dissertation research has been to elucidate how temporal filtering by single neurons contributes to the behavioral ability to recognize timing patterns in communication signals.

I have addressed this question using mormyrid weakly electric fish, which vary the time intervals between successive electric pulses to communicate. Fish detect these signals with sensory receptors in their skin. In the majority of species, these receptors fire a single spike in response to each electric pulse. Spiking receptors faithfully encode the interpulse intervals in communication signals into interspike intervals, which are then decoded by interval-selective midbrain neurons. Using in vivo intracellular recordings from awake fish during sensory stimulation, I found that short-term depression and temporal summation play important roles in establishing single-neuron interval selectivity. Moreover, the combination of short-term depression and temporal summation in the circuit resulted in greater diversity of interval tuning properties across the population of neurons, which would increase the population’s ability to detect temporally patterned communication signals. Indeed, I found that the responses of single interval-selective neurons were sensitive to subtle variation in the timing patterns of a specific communication display produced by different individuals.

A subset of mormyrid species has sensory receptors that produce spontaneously oscillating potentials. How the electrosensory system of these species established sensitivity to temporally patterned communication signals was completely unknown. Using in vivo extracellular recordings, I demonstrated that these receptors encode sensory stimuli into phase resets, which is the first clear instance of information coding by oscillatory phase reset. Furthermore, the ongoing oscillations conferred enhanced sensitivity to fast temporal patterns that are only found in the communication signals of a large group of fish. Behavioral playback experiments provided further support for the hypothesis that oscillating receptors are specialized for detecting communication signals produced by a group of conspecifics, which is a novel role for a sensory receptor. These findings demonstrate that temporal pattern sensitivity, which was previously thought to be a central processing problem, can also arise from peripheral filtering through a novel oscillatory phase reset mechanism.

Language

English (en)

Chair and Committee

Bruce A Carlson

Committee Members

Jeanne M Nerbonne, Timothy E Holy, Dennis L Barbour, Barani Raman,

Comments

Permanent URL: https://doi.org/10.7936/K7V98686

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