Chapter 1: Introduction and Background
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The Coding of Sound Localization Cues in the Inferior Colliculus by Steven M. Chase A dissertation submitted to Johns Hopkins University in conformity with the requirements for the degree of Doctor of Philosophy Baltimore, Maryland June 2006 © Steven M. Chase 2006 All rights reserved Abstract The auditory system uses three cues to decode sound location: interaural time differences (ITDs), interaural level differences (ILDs), and spectral notches (SNs). Initial processing of these cues is performed in several auditory brainstem nuclei that send projections to neurons of the inferior colliculus (IC). This work addresses how information about these different sound localization cues is integrated into the responses of single neurons of the IC. Virtual space techniques were used to create stimulus sets varying in two sound- localization parameters each. By manipulating pairs of cues within a stimulus set, the relative coding of each cue could be compared. Using a variety of information theoretic methods, the mutual information between the localization cues and the neural response was quantified under the assumption of several different encoding schemes. The results show that the three localization cues are best represented by different codes. ITD information is conveyed by spike rate alone, and is contained only in low frequency neurons. ILD information is best represented by a joint rate/first spike latency code. The coding of SNs changes with the best frequency (BF) of the neuron. Low BF neurons represent SNs by the timing of spikes distributed throughout the response, where the spike times are locked to particular stimulus features. High BF neurons, on the other hand, represent SNs by spike rate and, to a lesser extent, first spike latency. The differential coding of the localization cues suggests that information about multiple cues could be multiplexed onto the responses of single neurons. ii These results have implications for how the localization cues might be integrated into a percept of sound location. The accuracy with which each cue can contribute to the overall location percept changes depending on sound conditions, such as the frequency content of the stimulus, temporal characteristics of the stimulus, or the reverberant qualities of the environment. That the cues are differentially coded in the IC implies that the brain may have access to the individual cues at cortical levels, and the weight with which each cue contributes to the location percept could be tailored to the stimulus, environment, and perceptual task. Advisor Dr. Eric D. Young Professor Biomedical Engineering iii Acknowledgements Of course, I could never have completed this work on my own. My gratitude for the people whose patience, understanding, and insight helped me through this dissertation cannot adequately be expressed in words. I am indebted. My advisor, Eric Young, for giving me the guidance to get me going and the freedom to let me find my own way. Brad May, my second reader, who was always willing to answer questions and discuss results. Dissertation committee: Ed Connor, Xiaoqin Wang, and Kechen Zhang. NEL members, past and present, without whom this would have been a dreary and caffeine poor experience: Mike Anderson, Sharba Bandyopadhyay, Ian Bruce, Shanqing Cai, Kevin Davis, Gulam Emadi, Alon Fishbach, Mike Heinz, Ben Letham, Diana Ma, Lina Reiss, Tessa Ropp, Danilo Scepanovic, Zach Smith, William Tam, Phyllis Taylor, Anita Tilotta, Josh Vogelstein, and Jane Yu. My friends and family, who never admitted boredom when listening to the last result or setback. And finally, Anita Zuberi, who has always been a bottomless well of love and support. iv Table of Contents Title page.............................................................................................................................. i Abstract ...............................................................................................................................ii Acknowledgements ............................................................................................................ iv List of Tables.......................................................................................................x List of Figures .................................................................................................................... xi Chapter 1: Introduction and Background.........................................................1 1.1) Cues for sound localization.................................................................................... 3 1.2) Anatomy and physiology of sound localization nuclei.......................................... 4 1.2.1 – The ITD processing pathway ...................................................................... 4 1.2.2 – The ILD processing pathway ...................................................................... 6 1.2.3 – The SN processing pathway ........................................................................ 6 1.2.4 – Overlaps in the localization cue pathways.................................................. 7 1.3) Previous studies of the inferior colliculus relevant to sound localization ............. 8 1.3.1 – Physiological cell types within the inferior colliculus ................................ 8 1.3.2 – Sound location processing within the inferior colliculus............................ 9 1.4) Characterizing the responses of auditory neurons ............................................... 11 v Chapter 2: Methods................................................................................................. 14 2.1) Surgical procedure ............................................................................................... 14 2.2) Electrode fabrication............................................................................................ 16 2.3) Recording procedure............................................................................................ 17 2.4) Stimulus design.................................................................................................... 19 Chapter 3: Mutual Information and Bias Estimation ................................ 23 3.1) Overview.............................................................................................................. 24 3.2) Applying mutual information to neural encoding 26 3.3) Mutual information in two variables 28 3.3.1 – MI in two stimulus variables ..................................................................... 28 3.3.2 – MI in two response variables .................................................................... 30 3.4) Bounds and bias of mutual information estimates............................................... 31 3.5) Mutual information in spike rate 33 3.5.1 – Rate-based MI and the maximum likelihood estimate .............................. 33 3.5.2 – Debiasing schemes for rate-based MI estimates....................................... 34 3.5.3 – The fill-in method: a new debiasing technique ......................................... 39 3.6) Mutual information in a stimulus decoder 42 3.6.1 – Estimating MI from a hard partition decoder........................................... 43 3.6.2 – Debiasing confusion matrices ................................................................... 44 vi 3.7) Mutual information in first spike latency 47 3.7.1 – The breakdown of first spike latency information..................................... 48 3.7.2 – Kernel density estimates of MI.................................................................. 50 3.7.3 – Binless estimates of MI.............................................................................. 53 3.8) Derivation of the cue-interaction equation, Eqn. 3.13 56 3.9) Derivation of the first spike latency information equation, Eqn. 3.31 57 Chapter 4: Sound localization information encoded in spike rate......... 59 4.1) Overview of the data............................................................................................ 60 4.2) Rate responses to the SN/ILD and ITD/ILD stimulus sets 61 4.2.1 – The representation of single cues.............................................................. 61 4.2.2 – The representation of multiple cues .......................................................... 66 4.3) Responses to the ABI/ILD stimulus set 67 4.3.1 – Information about overall level vs. level differences ................................ 67 4.3.2 – Assessing monaural vs. binaural interactions: the Monaural Index ........ 69 4.4) Discussion of rate coding results 71 4.4.1 – Segregation of localization cue information among the IC cell types ...... 71 4.4.2 – Matching stimulus cues to neurons ........................................................... 73 4.4.3 – Comparison with other studies.................................................................. 74 4.5) Renormalization: correcting for slow drifts in neural excitability 75 vii Chapter 5: Sound localization information recovered by a decoder.... 78 5.1) The spike distance metric decoder....................................................................... 79 5.2) SDM analysis of the coding of individual localization cues 81 5.2.1 – Single-cue information .............................................................................. 81 5.2.2 – Time scale of information.......................................................................... 84 5.2.3 – Frozen vs. random noise ........................................................................... 85 5.3) SDM analysis of the coding of multiple