In partial fulfillment of the requirements for the degree of 

Doctor of Philosophy in Quantitative Biosciences

in the School of Biological Sciences

Joy Putney

Defends her thesis:
TEMPORAL ENCODING, PRECISION, AND COORDINATION IN A COMPREHENSIVE, SPIKE-RESOLVED MOTOR PROGRAM

Wednesday, September 22, 2021
1:15pm Eastern Time

Howey N201/202 and via BlueJeans: https://bluejeans.com/373892786/6839
Open to the Community

Advisor:

Dr. Simon Sponberg

School of Physics & School of Biological Sciences

Georgia Institute of Technology

Committee Members:
Dr. Young-Hui Chang; School of Biological Sciences, Georgia Tech

Dr. Hannah Choi; School of Mathematics, Georgia Tech
Dr. Ilya Nemenman; Department of Physics, Emory University
Dr. Garrett Stanley; Department of Biomedical Engineering, Georgia Tech & Emory University

Abstract:

Animals must execute robust, agile movement in a variety of biomechanical and environmental contexts. The nervous system must encode information for movement across multiple muscles in the "all-or-none" messages of action potentials. Sequences of action potentials, or spikes, can carry information in the number of spikes and their timing. Spike timing codes are critical in many sensory systems, but there is now growing evidence that millisecond-scale changes in timing also carry information in motor brain regions, descending decision-making circuits, and individual motor units. However, a thorough investigation of the importance of spike timing at the millisecond-scale for encoding information, coordinating muscles, and causally changing motor behavior would require recording a comprehensive, spike-resolved motor program across a complete set of muscles that actuate a behavior.

This work leverages the comprehensive, spike-resolved motor program of the hawk moth to demonstrate that the currency of motor control is millisecond-scale precise spike timings. We show that across the ten muscles that control the wings during flight, spike timing encodes more information about yaw torque than spike rate, and that spike timing encodes all coordinated information between pairs of muscles, despite there being sufficient bandwidth to encode the information in spike rate. We introduce a method to assess the necessary spike timing precision to encode information about behavior. In the comprehensive motor program of the hawk moth, the information encoded in spikes is precise to the millisecond or sub-millisecond scale, losing information when noise is added to spikes that exceeds several milliseconds. We demonstrate through classification that the motor program we record is indeed comprehensive, capable of near perfect classification of six types of behavior elicited in response to drifting visual stimuli as long as millisecond-scale information about spikes is available. Additionally, we demonstrate consistency in how muscles are coordinated across different types of behavior, though functionally different spiking activity occurs. Finally, we investigate specific precise spike timing differences observed in the six behavior types to demonstrate causality of millisecond-scale spike timing for behavior.