Proposed mechanisms for coincidence detection in the auditory brainstem

Sound localization in mammals uses two distinct neural circuits, one for low- and one for high-frequency bands. Recent experiments call for revision of the theory explaining how the direction of incoming sound is calculated. We propose such a revised theory. Our theory is based on probabilistic spiking and probabilistic delay of spikes from both sides. We have applied the mechanism originally proposed as an operation on spike trains resulting in multiplication of firing rates. We have adapted this mechanism for the case of synchronous spike trains. The mechanism has to detect spikes from both sides within a short time window. Therefore, in both circuits neurons act as coincidence detectors. In the excitatory low-frequency circuit we call the mechanism the excitatory coincidence detection, to distinguish it from the mechanism of the inhibitory coincidence detection in the high-frequency circuit. The times to first spike and gains of the two mechanisms are calculated. We show how the output gains of the mechanisms predict the dip within the human frequency sensitivity range. This dip has been described in human psychophysical experiments.

[1]  Guido Bugmann,et al.  Multiplying with neurons: Compensation for irregular input spike trains by using time-dependent synaptic efficiencies , 2004, Biological Cybernetics.

[2]  John H. R. Maunsell,et al.  On the relationship between synaptic input and spike output jitter in individual neurons. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[3]  R. Batra,et al.  Sensitivity to interaural temporal disparities of low- and high-frequency neurons in the superior olivary complex. I. Heterogeneity of responses. , 1997, Journal of neurophysiology.

[4]  Catherine E. Carr,et al.  Evolution of Time Coding Systems , 1999, Neural Computation.

[5]  D. McAlpine,et al.  A neural code for low-frequency sound localization in mammals , 2001, Nature Neuroscience.

[6]  Petr Marsalek,et al.  Neural code for sound localization at low frequencies , 2001, Neurocomputing.

[7]  Vladimír Majerník,et al.  Neural networks simulating the frequency discrimination of hearing for non-stationary short tone stimuli , 1996, Biological Cybernetics.

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

[9]  P. Joris,et al.  Detection of synchrony in the activity of auditory nerve fibers by octopus cells of the mammalian cochlear nucleus. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[10]  B. Grothe,et al.  Precise inhibition is essential for microsecond interaural time difference coding , 2002, Nature.

[11]  Gary D. Bernard,et al.  A proposed mechanism for multiplication of neural signals , 1976, Biological Cybernetics.

[12]  D. Tollin.  The Lateral Superior Olive: A Functional Role in Sound Source Localization , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[13]  P. Marsalek.  Coincidence detection in the Hodgkin-Huxley equations. , 2000, Bio Systems.

[14]  Petr Marsalek,et al.  Sound localization at high frequencies and across the frequency range , 2004, Neurocomputing.

[15]  J. Goldberg,et al.  Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. , 1969, Journal of neurophysiology.

[16]  Ramana Dodla,et al.  Subthreshold outward currents enhance temporal integration in auditory neurons , 2003, Biological Cybernetics.

[17]  R. Batra,et al.  Sensitivity to interaural temporal disparities of low- and high-frequency neurons in the superior olivary complex. II. Coincidence detection. , 1997, Journal of neurophysiology.

[18]  J. Rinzel,et al.  The role of dendrites in auditory coincidence detection , 1998, Nature.

[19]  P. Joris.  Envelope coding in the lateral superior olive. II. Characteristic delays and comparison with responses in the medial superior olive. , 1996, Journal of neurophysiology.

[20]  A. Reyes,et al.  Membrane properties underlying the firing of neurons in the avian cochlear nucleus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  Michael C. Reed,et al.  Precision of Neural Timing: Effects of Convergence and Time-Windowing , 2002, Journal of Computational Neuroscience.

[22]  T. Yin,et al.  Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. , 1995, Journal of neurophysiology.

[23]  T. Yin,et al.  Envelope coding in the lateral superior olive. III. Comparison with afferent pathways. , 1998, Journal of neurophysiology.

[24]  Krisztina Szalisznyó,et al.  Role of hyperpolarization-activated conductances in the auditory brainstem , 2004, Neurocomputing.

[25]  P. Marsalek,et al.  Spike encoding mechanisms in the sound localization pathway. , 2005, Bio Systems.

[26]  Petr Lánský,et al.  Sources of periodical force in noisy integrate-and-fire models of neuronal dynamics , 1997 .

[27]  A. Reyes,et al.  In vitro analysis of optimal stimuli for phase-locking and time-delayed modulation of firing in avian nucleus laminaris neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  L A JEFFRESS,et al.  A place theory of sound localization. , 1948, Journal of comparative and physiological psychology.

[29]  A.R.D. Thornton,et al.  Foundations of Modern Auditory Theory , 1970 .

[30]  R. Kempter,et al.  How the threshold of a neuron determines its capacity for coincidence detection. , 1998, Bio Systems.