Beyond timing in the auditory brainstem: intensity coding in the avian cochlear nucleus angularis

Abstract

IntroductionIndividual acoustic stimulus waveforms in the environment sum together to form a complex composite waveform that arrives at the ear as a single, time-varying pressure amplitude wave. The fundamental problem of hearing lies in how the brain decomposes that waveform into information useful for performing auditory tasks necessary for the survival of the animal such as sound localization and vocal communication. Many of the computational principles for sound localization have emerged from the study of avian brains, especially that of the barn owl, a specialized auditory predator . Additional data from less specialized birds, such as the chicken, and from mammals have revealed a suite of cellular and synaptic specializations in common for the temporal coding of sound, necessary for the detection of one important cue for localization, interaural time difference (ITD): fast glutamatergic neurotransmission, calyceal synaptic morphology, low-threshold voltagegated potassium conductances, bipolar dendritic structures, and axonal delay lines (Carr, 1993;Oertel, 1999;Trussell, 1999). Such commonalities of form arising in widely disparate animal clades suggest that there is a computational advantage to that form, whether it is dendritic structure, expression of a suite of ion channels, or the temporal patterning of activity. Brains in both birds and mammals experience similar constraints in detecting sound, and because hearing of airborne sound arose separately in these two groups, similarities in structure, function and coding between them suggest common coding principles at work, and common solutions arrived at through parallel evolution .A similarly comprehensive answer to the question of coding non-ITD aspects of sound has lagged behind. Early work in the barn owl recognized a division of labor for the coding of interaural timing differences versus interaural intensity differences (also known as interaural level differences, or ILDs), beginning with the two divisions of the avian cochlear nucleus: nucleus magnocellularis (NM) as the origin of the 'timing pathway' and nucleus angularis (NA) as the origin of the 'intensity pathway' ( Figure 1A) (Sullivan and Konishi, 1984;Takahashi et al., 1984); for review see. Both cochlear nuclei are monaural, and project to binaural targets which compare inputs from the two ears (Manley et al., 1988;Takahashi and Konishi, 1988). While NM neurons are similar to the mammalian cochlear nucleus bushy cells, NA is a heterogeneous nucleus with many properties similar to non-bushy cell components of the mammalian cochlear nucleus (CN) Köppl and Carr, 2003;Oertel, 1999;Soares and Carr, 2001;Soares et al., 2002). This heterogeneity (described below) coupled with the extreme specialization of one pathway for timing cues beginning with NM, suggests that NA is largely responsible for encoding non-localization aspects of sound in addition to its role in the ILD pathway. A major challenge will be to * Correspondence should be addressed to: Katrina MacLeod, Department of Biology, Universi...

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

“…Nucleus angularis appears to be the origin for everything else, although commonly referred to as the “intensity pathway”, which does not do justice to the complexity already seen at this level. The nucleus angularis contains a range of cell types having distinct anatomical and physiological properties [reviews in Fukui and Ohmori, 2003; Grothe et al, 2004; MacLeod and Carr, 2007]. Although cell-specific connection patterns have not been investigated, nucleus angularis neurons project to the superior olive and lemniscal nuclei, as well as directly to the auditory midbrain (inferior colliculus).…”

Heterogeneous Calretinin Expression in the Avian Cochlear Nucleus Angularis

“…The two anatomically distinct cochlear nuclei, nucleus magnocellularis (NM) and nucleus angularis (NA), each receive information from the auditory nerve and specialize for encoding timing information (NM) and intensity, or sound level, information (NA) for the computation of sound location (Boord 1968;Carr and Boudreau 1991;Parks and Rubel 1978;Puelles et al 2007;Reyes et al 1994;Sullivan and Konishi 1984;Trussell 1999). Nucleus angularis is highly heterogeneous in terms of neuronal morphology, acoustic response types in vivo and intrinsic physiology in vitro, and has multiple ascending projections, suggesting that it performs multiple functions Fukui and Ohmori 2003;Häusler et al 1999;Krützfeldt et al 2010a;MacLeod and Carr 2007;Sachs and Sinnott 1978;Sato et al 2010;Soares and Carr 2001;Soares et al 2002;Wang and Karten 2010;Warchol and Dallos 1990). The present study was undertaken to better define the molecular characterization of neurons in NA.…”

Short-term synaptic plasticity and intensity coding

“…The rich diversity of functional pathways in the auditory brain stem provides an opportunity to test the hypothesis that short-term plasticity is important for neural coding. Recent work in the brain stem nuclei of birds and mammals has provided evidence that short-term plasticity may contribute to the division of the pathways that encode temporal and intensity information for the purpose of sound localization (MacLeod & Carr, 2007; MacLeod et al, 2007). The auditory nerve bifurcates and projects to separate divisions of the cochlear nuclei where differences in the anatomy, morphology, physiology and short-term plasticity properties contribute to the parallel pathway divisions of acoustic information.…”

“…NM projects bilaterally only to nucleus laminaris (NL), creating a highly specialized circuit for the computation of ITD (Konishi, 2003). In contrast, NA neurons and response profiles have a diversity of functional types that bear a strong resemblance to those in the mammalian CN (Carr & Soares, 2002; Fukui & Ohmori, 2003; Köppl & Carr, 2003; MacLeod & Carr, 2007; Soares & Carr, 2001; Soares et al, 2002). Neurons in NA have four major projections: to the superior olivary nucleus (SON) in the brain stem, two lemniscal nuclei, and directly to the inferior colliculus (IC) in the midbrain.…”