The Superior Olivary Nucleus and Its Influence on Nucleus Laminaris: A Source of Inhibitory Feedback for Coincidence Detection in the Avian Auditory Brainstem

Abstract

Located in the ventrolateral region of the avian brainstem, the superior olivary nucleus (SON) receives inputs from nucleus angularis (NA) and nucleus laminaris (NL) and projects back to NA, NL, and nucleus magnocellularis (NM). The reciprocal connections between the SON and NL are of particular interest because they constitute a feedback circuit for coincidence detection. In the present study, the chick SON was investigated. In vivo tracing studies show that the SON projects predominantly to the ipsilateral NM, NL, and NA. In vitro whole-cell recording reveals single-cell morphology, firing properties, and postsynaptic responses. SON neurons are morphologically and physiologically suited for temporal integration; their firing patterns do not reflect the temporal structure of their excitatory inputs. Of most interest, direct stimulation of the SON evokes long-lasting inhibition in NL neurons. The inhibition blocks both intrinsic spike generation and orthodromically evoked activity in NL neurons and can be eliminated by bicuculline methiodide, a potent antagonist for GABAA receptor-mediated neurotransmission. These results strongly suggest that the SON provides GABAergic inhibitory feedback to laminaris neurons. We discuss a mechanism whereby SON-evoked GABAergic inhibition can influence the coding of interaural time differences for sound localization in the avian auditory brainstem.

Coding interaural time differences at low best frequencies in the barn owl

“…These results support the model in which the slope of the ITD function is used to encode sound location [71]. In birds, inhibitory inputs to nucleus laminaris are GABAergic, less temporally precise and appear to decrease excitability through a gain control mechanism that provides protection from changes in sound level [29,74,86,126]. Short-term synaptic plasticity may also contribute to coincidence detection [25].…”

Manipulation of inhibition in the owl’s nucleus laminaris and its effects on optic tectum neurons

“…Histochemical and neuropharmacological studies with slices have provided evidence for the presence of inhibitory transmitters such as GABA in the NL and glycine in the medial superior olive (Code et al, 1989;Code and Churchill, 1991;Carr and Boudreau, 1993;Lachica et al, 1994;Sanes, 1993, 1994;Hyson et al, 1995;Funabiki et al, 1998;Yang et al, 1999). Despite these observations the action of inhibitory transmitters in these nuclei has not been studied in vivo.…”

Modeling coincidence detection in nucleus laminaris

“…As a result, NL, primarily in chick and barn owl, has already been the objective of many anatomical (Rubel and Parks 1975;Smith and Rubel 1979;Smith 1981;Rubel 1984, 1989a, b) and electrophysiological experiments (Carr and Konishi 1990;Warchol and Dallos 1990;Overholt et al 1992;Pena et al 1996;Reyes et al 1996;Viete et al 1997;Bruckner and Hyson 1998;Funabiki et al 1998;Yang et al 1999;Monsivais et al 2000;Pena et al 2001;Kuba et al 2002;Cook et al 2003). This wealth of information has also made it the target of several modeling efforts (Grün et al 1990;Agmon-Snir et al 1998;Dasika et al 1999;Simon et al 1999a, b;Dasika et al 2001;Simon et al 2001a, b;Cook et al 2003;Carr et al in press).…”

“…Unlike the fast, phase-locked inhibitory input in mammalian MSO (Brand et al 2002), inhibitory input to NL is slow and not phase-locked (Funabiki et al 1998;Yang et al 1999;Monsivais et al 2000). The input to the inhibitory synapses is from a modeled superior olivary nucleus (SON) (Takahashi and Konishi 1988;Carr et al 1989;Lachica et al 1994).…”

“…Tables 2 and 8). The inhibitory parameters for these simulations use a reversal potential hyperpolarized with respect to the resting potential (-80 mV), but a depolarized reversal potential of -60 mV (accompanied by a doubling of the conductance to give the same effective driving force) produced almost identical behavior (see Bruckner and Hyson 1998;Funabiki et al 1998;Yang et al 1999;Monsivais et al 2000).…”