Effects of Inhibitory Feedback in a Network Model of Avian Brain Stem

Abstract

. Effects of inhibitory feedback in a network model of avian brain stem. J Neurophysiol 94: 400 -414, 2005. First published March 2, 2005; doi:10.1152/jn.01065.2004. The avian auditory brain stem consists of a network of specialized nuclei, including nucleus laminaris (NL) and superior olivary nucleus (SON). NL cells show sensitivity to interaural time difference (ITD), a critical cue that underlies spatial hearing. SON cells provide inhibitory feedback to the rest of the network. Empirical data suggest that feedback inhibition from SON could increase the ITD sensitivity of NL across sound level. Using a bilateral network model, we assess the effects of SON feedback inhibition. Individual cells are specified as modified leakyintegrate-and-fire neurons with time constants and thresholds that vary with inhibitory input. Acoustic sound level is reflected in the discharge rates of the model auditory-nerve fibers, which innervate the network. Simulations show that with SON inhibitory feedback, ITD sensitivity is maintained in model NL cells over a threefold range in auditory-nerve discharge rate. In contrast, without SON feedback inhibition, ITD sensitivity is significantly reduced as input rates are increased. Feedback inhibition is most beneficial in maintaining ITD sensitivity at high-input rates (simulating high sound levels). With SON inhibition, ITD sensitivity is maintained for both interaurally balanced inputs (simulating an on-center sound source) and interaurally imbalanced inputs (simulating a lateralized source). Further, the empirically observed temporal build-up of SON inhibition and the presence of reciprocal inhibitory connections between the ipsi-and contralateral SON both improve ITD sensitivity. In sum, our network model shows that inhibitory feedback can substantially increase the sensitivity and dynamic range of ITD coding in the avian auditory brain stem. I N T R O D U C T I O NThe submillisecond difference in the time of arrival of sound to the two ears, interaural time difference (ITD), is a critical cue in the localization and processing of sound sources (cf. Blauert 1997). Nucleus laminaris (NL), the avian homologue of the mammalian medial superior olive (MSO), is the first neural center to receive input from the two ears. Fibers from nucleus magnocellularis (NM) project bilaterally and provide phase-locked, glutamatergic, excitatory input to NL. Single neurons in NL show sensitivity to ITD by performing coincidence detection (Jeffress 1948) on the input from left and right NM (Carr and Konishi 1990;Sullivan and Konishi 1984). Empirical data indicate that ITD sensitivity is maintained in NL over a 50-dB range in sound level (Peña et al. 1996). However, simple coincidence models (Peña et al. 1996; Reed and Durbeck 1995) lose ITD sensitivity as the discharge rate of NM fibers monotonically increases threefold or more with sound level (Warchol and Dallos 1990).Two mechanisms have been demonstrated to maintain ITD sensitivity in models of NL despite variations in sound level. First, synaptic d...

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).…”

Endogenous mGluR Activity Suppresses GABAergic Transmission in Avian Cochlear Nucleus Magnocellularis Neurons

“…GABA inhibits glutamate release at a presynaptic locus by metabotropic GABA B Rs (Brenowitz and Trussell 2001;Brenowitz et al 1998;Otis and Trussell 1996). Neurons in the superior olivary nucleus (SON), driven by excitatory inputs from nucleus laminaris (NL) and nucleus angularis (NA), probably fire in a sound level-dependent manner Dasika et al 2005). That is, stronger excitatory glutamatergic inputs to the avian cochlear nucleus lead to stronger feedback inhibitory inputs.…”

“…The GABAergic inputs enhance phase-locking fidelity of NM neurons in response to auditory inputs and thus improve the ability of NM neurons to code timing information of sound stimuli (Monsivais et al 2000). The GABAergic inputs are also proposed to function as a gain control for the excitatory inputs to NM Dasika et al 2005).…”

Frequency Dependent Specialization for Processing Binaural Auditory Cues in Avian Sound Localization Circuits

“…Loud sound was expected to reduce the peak-trough contrast by simulation (Dasika et al, 2005). However, the peaktrough contrast was maintained rather at high sound pressure level in the barn owl (Pena et al, 1996).…”

“…The simulation further showed that without balance in the bilateral excitation, the peak-trough contrast of ITD tuning lost tolerance to the loud sounds. The SON inhibition might also play a role in maintaining the balance of excitation from NM on the two sides (Dasika et al, 2005). …”