Bilateral inhibition generates neuronal responses tuned to interaural level differences in the auditory brainstem of the barn owl

Abstract

I investigated the neural algorithms by which neurons gain selectivity for interaural level difference in the brainstem of the barn owl (Tyto alba). Differences in the timing and in the level of sounds at the ears are used by this owl to encode, respectively, azimuthal and vertical position of sound sources in space. These two cues are processed in two parallel neural pathways. Below the level of the inferior colliculus, all neurons in the pathway that processes level differences show responses to this cue that are monotonic, and thus not selective for a particular level difference. Only in the inferior colliculus, which contains a map of auditory space, are neurons sharply tuned to specific interaural level differences. How are these response properties generated from those of the nuclei that provide input to the inferior colliculus? I show that the posterior subdivision of the nucleus ventralis lemnisci lateralis (VLVp) projects bilaterally to the lateral shell of the central nucleus of the inferior colliculus, the input stage to the map of auditory space. Both these nuclei are part of the pathway that processes interaural level differences. Manipulations of the responses in VLVp affected the responses to level differences in the inferior colliculus; responses to time differences were unaffected. By systematically increasing or decreasing neural activity in VLVp, I show that the VLVp on each side provides inhibition to the colliculus at large level differences. This results in a peaked response that is tuned to level differences in the inferior colliculus. Some cells in the lateral shell of the inferior colliculus appear to receive direct GABAergic inhibition from VLVp. I suggest that this circuitry and the algorithms it supports are the neural substrates that allow the barn owl to exploit level differences for computation of sound source elevation.

Stimulus-specific adaptation, habituation and change detection in the gaze control system

“…3). This similarity is especially striking taking into account that the four features are represented and computed in markedly different ways: ITD and ILD, the two primary binaural localization cues, are processed in parallel in two separate and independent brainstem pathways (Takahashi et al 1984;Takahashi and Konishi 1988;Adolphs 1993;Albeck and Konishi 1995); frequency separation is maintained in both ascending auditory pathways from the cochlea up to the level of the lateral shell of the inferior colliculus where information across frequency-specific channels is combined (Euston and Takahashi 2002). Sound-level information is presumably manifested in the response levels of the ascending pathways.…”

Stimulus-Specific Adaptations in the Gaze Control System of the Barn Owl

“…9, 10, 13) and the adaptation memory was at least 1 s long (we did not attempt other ISIs). This similarity is especially striking taking into account that the four features are represented and computed in marginally different ways: ITD and ILD, the two primary binaural localization cues, are processed in parallel in two separate and independent brainstem pathways that converge in the lateral shell of the central nucleus of the inferior colliculus (ICCls) (Takahashi et al, 1984;Takahashi and Konishi, 1988;Adolphs, 1993;Albeck and Konishi, 1995) to induce selectivity to spatial locations, which is then further refined along the pathway to the ICX and on to the OT (Moiseff and Konishi, 1983;Pena and Konishi, 2001). Frequency separation is maintained in both ascending auditory pathways from the cochlea up to the level of the ICCls where information across frequency-specific channels is combined (Euston and Takahashi, 2002).…”

Heterogeneous Calretinin Expression in the Avian Cochlear Nucleus Angularis

“…NM specializes in encoding fine timing cues and projects to the binaural nucleus responsible for computing ITD, NL (Carr and Konishi 1990;Fukui et al 2006;Hackett et al 1982;Koyano et al 1996;Nishino et al 2008;Raman et al 1994;Reyes et al 1994;Smith 1981;Trussell 1999;Zhang and Trussell 1994). Sound intensity cues for interaural level differences are processed first in NA which projects to the binaural nucleus responsible for computing ILD (Adolphs 1993;Manley et al 1988;Sato et al 2010;Sullivan and Konishi 1984;Takahashi et al 1984). Both NA and NL send a direct projections FIG.…”