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Spike Transmission Delay at the Calyx of Held In Vivo: Rate Dependence, Phenomenological Modeling, and Relevance for Sound Localization

¹Institute of Biology II and ³ Institute for Mathematics, University of Leipzig; and ² Max Planck Institute for Mathematics in the Sciences, Leipzig, Germany

Submitted 27 March 2009; accepted in final form 9 June 2009

Transmission at central synapses exhibits rapid changes in response amplitude under different patterns of stimulation. Whether the delay associated with the transmission of action potentials is similarly modifiable is important for temporally precise computations. We address this question at the calyx of Held of the medial nucleus of the trapezoid body (MNTB) in Mongolian gerbils in vivo using extracellular recordings. Here the pre- and postsynaptic activity can be observed simultaneously, allowing the definition of an action potential transmission delay (ATD) from the pre- to the postsynaptic side. We find the ATD to increase as a function of spike rate (10–40%). The temporal dynamics of the ATD increase exhibit an exponential shape with activity-dependent time constants (15–25 ms). Recovery dynamics of ATD were mono- (20–70 ms) or biexponential with fast (3–20 ms) and slow time constants (50–500 ms). Using a phenomenological model to capture ATD dynamics, we estimated ATD = 5–30 µs per transmitted action potential. Using vocalizations and cage noise stimuli, we confirm that substantial changes in ATD occur in natural situations. Because the ATD changes cover the behaviorally relevant range of interaural time differences in gerbils, these results could provide constraints for models of sound localization.