Avian superior olivary nucleus provides divergent inhibitory input to parallel auditory pathways

Abstract

The avian auditory brainstem displays parallel processing, a fundamental feature of vertebrate sensory systems. Nuclei specialized for temporal processing are largely separate from those processing other aspects of sound. One possible exception to this parallel organization is the inhibitory input provided by the superior olivary nucleus (SON) to nucleus angularis (NA), nucleus magnocellularis (NM), and nucleus laminaris (NL) and contralateral SON (SONc). We sought to determine whether single SON neurons project to multiple targets or separate neuronal populations project independently to individual target nuclei. We introduced two different fluorescent tracer molecules into pairs of target nuclei and quantified the extent to which retrogradely labeled SON neurons were double labeled. A large proportion of double-labeled SON somata were observed in all cases in which injections were made into any pair of ipsilateral targets (NA and NM, NA and NL, or NM and NL), suggesting that many individual SON neurons project to multiple targets. In contrast, when injections involved the SONc and any or all of the ipsilateral targets, double labeling was rare, suggesting that contralateral and ipsilateral targets are innervated by distinct populations of SON neurons arising largely from regionally segregated areas of SON. Therefore, at the earliest stages of auditory processing, there is interaction between pathways specialized to process temporal cues and those that process other acoustic features. We present a conceptual model that incorporates these results and suggest that SON circuitry, in part, functions to offset interaural intensity differences in interaural time difference processing.

Interaural Time Difference Processing in the Mammalian Medial Superior Olive: The Role of Glycinergic Inhibition

“…It therefore seems conceivable that the hyperpolarizing inhibitory inputs in the MSO help to convey intensity robustness of ITD sensitivity by defining the binaural coincidence window and preventing outof-phase responses, which otherwise increase in likelihood at higher intensities (Reed and Durbeck, 1995). Such gain control is also present in the avian analog of the MSO; however, it is achieved by tonic, GABAergic inputs providing depolarizing, shunting inhibition (Yang et al, 1999;Burger et al, 2005;Dasika et al, 2005).…”

Computation of Interaural Time Difference in the Owl's Coincidence Detector Neurons

“…GABAergic inhibition (Carr et al, 1989;Lachica et al, 1994;Funabiki et al, 1998;Yang et al, 1999;Burger et al, 2005) and synaptic depression (Kuba et al, 2002;Cook et al, 2003;Slee et al, 2010) are candidates for sound-induced suppression mechanisms of synaptic inputs in NL. In our experimental observation, sound-evoked DC shifts did not change with ITD (Figs.…”

Sound-Intensity-Dependent Compensation for the Small Interaural Time Difference Cue for Sound Source Localization

“…In birds, the fast inhibitory neurons like the principal cells of MNTB do not exist in the ITD processing circuit, whereas around the perikaryon and proximal dendrites of NL are concentrated GABA terminals (Carr et al, 1989;Code et al, 1989). The major source of these terminals is the superior olivary nucleus (SON), which receives the input proportional to the sound intensity from the nucleus angularis (NA), and makes an inhibitory innervation to NL (Lachica et al, 1994;Yang et al, 1999;Burger et al, 2005). Moreover, GABA is reported to facilitate coincidence detection from the findings in in vitro experiments in NL (Hyson et al, 1995;Funabiki et al, 1998).…”

“…By simulation, the inhibition from SON is proposed to increase the threshold of neural activity in NL of the barn owl to make the ITD sensitivity tolerant to the sound intensity (Peña et al, 1996). It is suggested further that SON activity may balance the effects of interaural intensity difference in processing ITD (Burger et al, 2005;Dasika et al, 2005). Although various compensatory functions of SON activity have been proposed so far, it is still not clear how these functions actually shape the ITD tuning of NL neurons in a living animal.…”

“…The electrode was made by inserting a heavy-polyimide-coated tungsten wire (15 m diameter; California Fine Wire) into a microelectrode made from a glass capillary of 1.5 mm outer diameter (GD-1.5; Narishige); the resistance was ϳ1 M⍀, and the wire tip protruded ϳ10 m from the capillary tip of 20 -30 m diameter At the location where the largest auditory response was recorded, a lesion or labeling of SON was made. Because SON neurons are known to project mainly to ipsilateral NL, NA, and NM (Monsivais et al, 2000;Burger et al, 2005), we lesioned SON ipsilateral to NL recording sites by passing a constant current of 50 A for 100 s. We began unit recordings 1 h later. In SON labeling, the glass pipette was filled with PBS containing recombinant Sindbis virus expressing a fluorescent protein mRFP1 (monomeric red fluorescent protein) (courtesy of Dr. R. Y. Tsien, University of California, San Diego, La Jolla, CA) with a membrane-targeted palmitoylation signal of GAP43 (Furuta et al, 2001); the virus was designed by and the cDNA was provided by H. Hioki, T. Furuta, and T. Kaneko.…”