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.

Keywords: adaptation; auditory; central nucleus of the inferior colliculus; frequency tuning; interaural level difference; interaural time difference; plasticity; sound localization.

Figure 1

Auditory pathway. The afferent auditory pathway is schematically illustrated starting from the auditory nerve upstream to the optic tectum (OT) where the auditory and visual maps merge. Nuclei mentioned in black transmit only ITD information (black solid lines) whereas nuclei indicated in white underlie processing of ILDs and their precursors only (dashed lines and italics). Nuclei shown in gray are involved in the processing of both ITD and ILD information.

Figure 2

IC anatomy. A horizontal section through IC with the four important sub-nuclei. Photograph from a staining with Calbindin. V, ventricle; a, anterior; m, medial.

Figure 3

ITD tuning. Shown are examples of the variations of the normalized responses with ITD of neurons located in different sub-nuclei of the IC. The stimulus for collecting these tuning curves was broadband noise. ITD tuning is periodic in the ICCc with the distance of the peaks reflecting the best frequency of the neuron (A). All peaks have a similar height. A similar tuning is observed in the cells of the ICCls (B). By contrast in the responses of the cells of the ICX one peak, the main peak, is clearly dominant compared to the other peaks, the side peaks (C).

Figure 4

Distribution of interaural phase difference in low-best frequency neurons of ICCc. Distribution of 251 data points. Interaural phase differences were calculated from interaural time differences by first restricting the mean interaural phase differences to a range from −0.5 to 0.5 cycles by phase wrapping and then take the absolute value. A binwidth of 0.0625 and of 268 Hz was chosen to make the data comparable to the model data of Harper and McAlpine (2004).

Figure 5

Frequency tuning. Shown are examples of the variations of the normalized responses with frequency of neurons located in different nuclei of the IC. In ICCc frequency tuning is narrow (A). A similar tuning is observed in the cells of ICCls (B). By contrast frequency tuning of the cells of the ICX is broader than in ICC (C).

Figure 6

ILD tuning. Shown are examples of the variations of the normalized responses with ILD of neurons located in different nuclei of the IC. The responses of ICCc cells do not vary with the interaural level difference (ILD) (A). The ILD tuning of the cells in ICCls is sigmoidal (B), while the ILD tuning in ICX is bell-shaped (C).

Figure 7

A multiplicative receptive field of an ICX neuron. The response of this cell depends on ITD, which correlates with azimuth and on ILD, which correlates with elevation. Note that the responses in the two orthogonal directions, azimuth and elevation, are independent, because the shape of the curve of one parameter remains constant as the other parameter is changed. Only the height of the peak changes.

Figure 8

Schematic representation of the mid-brain auditory localization pathway in normal and in prism-reared owls. The inset shows a lateral view of the barn owl's brain. The line marks the approximate plane of the section through the tectal lobe illustrated schematically in A and B. (A) Information flows from the central nucleus of the inferior colliculus (ICC) to the external nucleus of the inferior colliculus (ICX) and from there to the optic tectum (OT). A map of auditory space is created in ICX. This map joins the visual retinotopic map arriving from the retina and forebrain in OT. Topographic connections from the OT to the ICX presumably carry spatial visual information to instruct auditory plasticity in the ICX (dotted arrows). The circled numbers in the ICX and OT represent the azimuthal positions in space to which the neurons are tuned to. (B) Following a period of several weeks of prism adaptation the axonal connections between the ICC and the ICX grow in an abnormal pattern. Connections are shifted to the rostral direction in one side of the brain and to the caudal direction in the other side of the brain. This pattern of axonal re-growth shifts the auditory maps in the ICX and the OT to align with the shifted visual map.

Figure 9

Adaptation in ICC. The response ratio, defined as the quotient of the unit's response rate to a given probe (second stimulus), divided by the response rate of a particular reference-stimulus (first stimulus), is plotted. (A) The mean response ratios as a function of the relative reference-stimulus level. Probe and reference stimulus had the same level. The reference level refers to the dynamic range as determined from the rate-level function (RLF). The responses ratios decreased with decreasing reference level and differed significantly between 90 and 10% reference-stimulus level (Mann–Whitney test, P < 0.0001). (B) Responses ratios as a function of the interstimulus interval (ISI) tested. Response ratios were significantly reduced compared with unity for ISIs up to 400 ms (one-sample t-tests, all P < 0.05; significance levels are indicated as follows: P < 0.05: ^*; P < 0.01: ^**; P < 0.001: ^***). The recovery function could be fitted well (R² = 0.982) by a double exponential with a short time constant of 1.25 ms and a long time constant of 800 ms (see inset in B).