The Role of Conduction Delay in Creating Sensitivity to Interaural Time Differences.

Axons from the nucleus magnocellularis (NM) and their targets in nucleus laminaris (NL) form the circuit responsible for encoding interaural time difference (ITD). In barn owls, NL receives bilateral inputs from NM, such that axons from the ipsilateral NM enter NL dorsally, while contralateral axons enter from the ventral side. These afferents act as delay lines to create maps of ITD in NL. Since delay-line inputs are characterized by a precise latency to auditory stimulation, but the postsynaptic coincidence detectors respond to ongoing phase difference, we asked whether the latencies of a local group of axons were identical, or varied by multiples of the inverse of the frequency they respond to, i.e., to multiples of 2π phase. Intracellular recordings from NM axons were used to measure delay-line latencies in NL. Systematic shifts in conduction delay within NL accounted for the maps of ITD, but recorded latencies of individual inputs at nearby locations could vary by 2π or 4π. Therefore microsecond precision is achieved through sensitivity to phase delays, rather than absolute latencies. We propose that the auditory system "coarsely" matches ipsilateral and contralateral latencies using physical delay lines, so that inputs arrive at NL at about the same time, and then "finely" matches latency modulo 2π to achieve microsecond ITD precision.

[1]  Richard Kempter,et al.  Maps of ITD in the nucleus laminaris of the barn owl. , 2013, Advances in experimental medicine and biology.

[2]  L. Carney,et al.  Temporal coding of resonances by low-frequency auditory nerve fibers: single-fiber responses and a population model. , 1988, Journal of neurophysiology.

[3]  Hermann Wagner,et al.  A functional circuit model of interaural time difference processing. , 2014, Journal of neurophysiology.

[4]  M. Konishi,et al.  Computation of Interaural Time Difference in the Owl's Coincidence Detector Neurons , 2011, The Journal of Neuroscience.

[5]  Philip X Joris,et al.  Oscillatory Dipoles As a Source of Phase Shifts in Field Potentials in the Mammalian Auditory Brainstem , 2010, The Journal of Neuroscience.

[6]  Richard Kempter,et al.  Auditory responses in the barn owl's nucleus laminaris to clicks: impulse response and signal analysis of neurophonic potential. , 2009, Journal of neurophysiology.

[7]  Catherine E. Carr,et al.  Biophysical basis of the sound analog membrane potential that underlies coincidence detection in the barn owl , 2013, Front. Comput. Neurosci..

[8]  L H Carney,et al.  Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. , 1994, Journal of neurophysiology.

[9]  M. Konishi,et al.  A circuit for detection of interaural time differences in the brain stem of the barn owl , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  M Konishi,et al.  Cellular mechanisms for resolving phase ambiguity in the owl's inferior colliculus. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[11]  L. Robles,et al.  Basilar-membrane responses to tones at the base of the chinchilla cochlea. , 1997, The Journal of the Acoustical Society of America.

[12]  Richard Kempter,et al.  On the origin of the extracellular field potential in the nucleus laminaris of the barn owl (Tyto alba). , 2010, Journal of neurophysiology.

[13]  Richard Kempter,et al.  Linear summation in the barn owl's brainstem underlies responses to interaural time differences. , 2013, Journal of neurophysiology.

[14]  E D Young,et al.  Discharge patterns of single fibers in the pigeon auditory nerve. , 1974, Brain research.

[15]  José Luis Peña,et al.  Noise Reduction of Coincidence Detector Output by the Inferior Colliculus of the Barn Owl , 2006, The Journal of Neuroscience.

[16]  D. Sanes,et al.  The sharpening of frequency tuning curves requires patterned activity during development in the mouse, Mus musculus , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  C. Köppl,et al.  Frequency tuning and spontaneous activity in the auditory nerve and cochlear nucleus magnocellularis of the barn owl Tyto alba. , 1997, Journal of neurophysiology.

[18]  Richard Kempter,et al.  Microsecond precision of phase delay in the auditory system of the barn owl. , 2005, Journal of neurophysiology.

[19]  L. Carney,et al.  Frequency glides in the impulse responses of auditory-nerve fibers. , 1999 .

[20]  Wulfram Gerstner,et al.  A neuronal learning rule for sub-millisecond temporal coding , 1996, Nature.

[21]  W. Shofner,et al.  Regularity and latency of units in ventral cochlear nucleus: implications for unit classification and generation of response properties. , 1988, Journal of neurophysiology.

[22]  H. Wagner,et al.  Representation of interaural time difference in the central nucleus of the barn owl's inferior colliculus , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  David J. Anderson,et al.  Temporal Position of Discharges in Single Auditory Nerve Fibers within the Cycle of a Sine‐Wave Stimulus: Frequency and Intensity Effects , 1971 .

[24]  José Luis Peña,et al.  Cross-Correlation in the Auditory Coincidence Detectors of Owls , 2008, The Journal of Neuroscience.

[25]  Mario A. Ruggero,et al.  Basilar Membrane Motion and Spike Initiation in the Cochlear Nerve , 1986 .

[26]  M. Konishi,et al.  Neural map of interaural phase difference in the owl's brainstem. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Wulfram Gerstner,et al.  Extracting Oscillations: Neuronal Coincidence Detection with Noisy Periodic Spike Input , 1998, Neural Computation.

[28]  Edwin W Rubel,et al.  Mechanisms for Adjusting Interaural Time Differences to Achieve Binaural Coincidence Detection , 2010, The Journal of Neuroscience.

[29]  Christine Köppl,et al.  Maps of interaural time difference in the chicken’s brainstem nucleus laminaris , 2008, Biological Cybernetics.