The representation of sound localization cues in the barn owl's inferior colliculus

Abstract

The barn owl is a well-known model system for studying auditory processing and sound localization. This article reviews the morphological and functional organization, as well as the role of the underlying microcircuits, of the barn owl's inferior colliculus (IC). We focus on the processing of frequency and interaural time (ITD) and level differences (ILD). We first summarize the morphology of the sub-nuclei belonging to the IC and their differentiation by antero- and retrograde labeling and by staining with various antibodies. We then focus on the response properties of neurons in the three major sub-nuclei of IC [core of the central nucleus of the IC (ICCc), lateral shell of the central nucleus of the IC (ICCls), and the external nucleus of the IC (ICX)]. ICCc projects to ICCls, which in turn sends its information to ICX. The responses of neurons in ICCc are sensitive to changes in ITD but not to changes in ILD. The distribution of ITD sensitivity with frequency in ICCc can only partly be explained by optimal coding. We continue with the tuning properties of ICCls neurons, the first station in the midbrain where the ITD and ILD pathways merge after they have split at the level of the cochlear nucleus. The ICCc and ICCls share similar ITD and frequency tuning. By contrast, ICCls shows sigmoidal ILD tuning which is absent in ICCc. Both ICCc and ICCls project to the forebrain, and ICCls also projects to ICX, where space-specific neurons are found. Space-specific neurons exhibit side peak suppression in ITD tuning, bell-shaped ILD tuning, and are broadly tuned to frequency. These neurons respond only to restricted positions of auditory space and form a map of two-dimensional auditory space. Finally, we briefly review major IC features, including multiplication-like computations, correlates of echo suppression, plasticity, and adaptation.

Binaural responses in the auditory midbrain of chicken (Gallus gallus)

“…The prominence of contralateral responses is consistent with the known projection patterns in chickens (Wang & Karten, ) and in pigeons (Boord, ). Typically, avian IC has been found to be the merging region of the two binaural pathways, such that both ITD and ILD sensitivities are expected to be represented (e.g., pigeon: Lewald, ; barn owl: Singheiser et al ., ; chicken: Coles & Aitkin, ) and were also found in the present study. Finally, the positive correlation between best frequency and tuning bandwidth was observed in chickens as well as in barn owls (Wagner et al ., ), and mirrors a well‐known, general relationship already established at the level of the auditory nerve (reviewed in Gleich & Manley, ) and presumably perpetuated up to the IC.…”

“…The principal response types in chicken IC depicted by our study are broadly consistent with earlier findings in other birds, including the barn owl. A majority of frequency‐selective sites have been found in the auditory midbrain of the chicken (Coles & Aitkin, ), pigeon (Lewald, ), zebra finch (Woolley & Casseday, ), birds of prey (Calford et al ., ) and barn owl (review in Singheiser et al ., ). The prominence of contralateral responses is consistent with the known projection patterns in chickens (Wang & Karten, ) and in pigeons (Boord, ).…”

“…The presence of both types is consistent with bilateral projections from LLDp (in the barn owl; Adolphs, ). In the barn owl, such simple sigmoid ILD responses are considered to be an intermediate step towards narrowly selective ILD tuning in the ICX (reviews in Konishi, ; Singheiser et al ., ). Their representation in other parts of the owl's IC remains poorly explored (Wagner et al ., ), and their functional role within the IC is unclear.…”

“…Three of the 4 units were not frequency‐selective. These features closely match the characteristics of units in the owls’ ICX (review in Singheiser et al ., ). Verification of recording sites is now necessary to clarify whether these units are also located in ICX‐like regions in non‐owl species.…”

“…Finally, the segregated and topographic ITD and ILD representations project convergently to the external nucleus of IC (ICX), generating a map of auditory space (Knudsen & Konishi, 1978a). IC in general plays a crucial role in sound perception, as most auditory information must pass through it before reaching the forebrain nuclei (reviewed in Casseday et al, 2002;Carr & Code, 2000;Singheiser et al, 2012). So far, the auditory pathway of the barn owl is arguably the most extensively studied of all species as a model for binaural information processing and sound localization.…”