A circuit for detection of interaural time differences in the brain stem of the barn owl

Abstract

Detection of interaural time differences underlies azimuthal sound localization in the barn owl Tyto alba. Axons of the cochlear nucleus magnocellularis, and their targets in the binaural nucleus laminaris, form the circuit responsible for encoding these interaural time differences. The nucleus laminaris receives bilateral inputs from the cochlear nucleus magnocellularis such that axons from the ipsilateral cochlear nucleus enter the nucleus laminaris dorsally, while contralateral axons enter from the ventral side. This interdigitating projection to the nucleus laminaris is tonotopic, and the afferents are both sharply tuned and matched in frequency to the neighboring afferents. Recordings of phase-locked spikes in the afferents show an orderly change in the arrival time of the spikes as a function of distance from the point of their entry into the nucleus laminaris. The same range of conduction time (160 mu sec) was found over the 700-mu m depth of the nucleus laminaris for all frequencies examined (4-7.5 kHz) and corresponds to the range of interaural time differences available to the barn owl. The estimated conduction velocity in the axons is low (3-5 m/sec) and may be regulated by short internodal distances (60 mu m) within the nucleus laminaris. Neurons of the nucleus laminaris have large somata and very short dendrites. These cells are frequency selective and phase-lock to both monaural and binaural stimuli. The arrival time of phase-locked spikes in many of these neurons differs between the ipsilateral and contralateral inputs. When this disparity is nullified by imposition of an appropriate interaural time difference, the neurons respond maximally. The number of spikes elicited in response to a favorable interaural time difference is roughly double that elicited by a monaural stimulus. Spike counts for unfavorable interaural time differences fall well below monaural response levels. These findings indicate that the magnocellular afferents work as delay lines, and the laminaris neurons work as co-incidence detectors. The orderly distribution of conduction times, the predictability of favorable interaural time differences from monaural phase responses, and the pattern of the anatomical projection from the nucleus laminaris to the central nucleus of the inferior colliculus suggest that interaural time differences and their phase equivalents are mapped in each frequency band along the dorsoventral axis of the nucleus laminaris.

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

“…In general, changes in delay with depth were consistent with the NM axons acting as delay lines (Carr and Konishi 1990), and with modelled conduction velocities in McColgan et al (2014). Ipsilateral recordings showed an increase in latency with recording depth in NL (open symbols in Fig.…”

“…d Most data from 3 penetrations through NL ( n = 38 units, 2 owls) showed systematic shifts in latency with recording depth, consistent with models of delay (see 2b, lumped in 0 µs bin). Other units were 2π or 4π or later than neighbouring units (c, arrows) ments from previous studies (Carr and Konishi 1990). Nevertheless, we point out that while these depth-dependent changes in delay would be expected from multiple recordings from the same NM axon, they were not required for ITD sensitivity.…”

“…This coding strategy remains viable for non-periodic sounds because the tonotopic organization of the auditory system generates ringing properties of the inputs characteristic of the particular frequency (Carney et al 1999;Recio et al 1998;Wagner et al 2005). Previously we had shown that the inputs from the cochlear nuclei act as delay line inputs to form maps of ITD in the barn owl (Carr and Konishi 1990), but could not determine whether the delay lines had identical conduction latencies or were matched for phase only.…”

Development of NMDA R1 expression in chicken auditory brainstem

“…The NM axons act as delay lines to construct a map of interaural time differences in NL (Carr and Konishi, 1990;Overholt et al, 1992;Kuba et al, 2002). NR1 and NR2B mRNA first appear in NL before E10, when the NL cells are aligned in a compact layer.…”

Reverse Correlation Analysis of Auditory-Nerve Fiber Responses to Broadband Noise in a Bird, the Barn Owl

“…The fact that delays could depend on input level is very important for interaural time difference (ITD) processing (Michelet et al 2012), for which the barn owl is a specialist (Carr and Konishi 1990). In the barn owl, ITD processing is thought to be based on a cross correlation (Fischer et al 2008).…”