Comparison of midbrain and thalamic space-specific neurons in barn owls

Abstract

Spatial receptive fields of neurons in the auditory pathway of the barn owl result from the sensitivity to combinations of interaural time (ITD) and level differences across stimulus frequency. Both the forebrain and tectum of the owl contain such neurons. The neural pathways, which lead to the forebrain and tectal representations of auditory space, separate before the midbrain map of auditory space is synthesized. The first nuclei that belong exclusively to either the forebrain or the tectal pathways are the nucleus ovoidalis (Ov) and the external nucleus of the inferior colliculus (ICx), respectively. Both receive projections from the lateral shell subdivision of the inferior colliculus but are not interconnected. Previous studies indicate that the owl's tectal representation of auditory space is different from those found in the owl's forebrain and the mammalian brain. We addressed the question of whether the computation of spatial cues in both pathways is the same by comparing the ITD tuning of Ov and ICx neurons. Unlike in ICx, the relationship between frequency and ITD tuning had not been studied in single Ov units. In contrast to the conspicuous frequency independent ITD tuning of space-specific neurons of ICx, ITD selectivity varied with frequency in Ov. We also observed that the spatially tuned neurons of Ov respond to lower frequencies and are more broadly tuned to ITD than in ICx. Thus there are differences in the integration of frequency and ITD in the two sound-localization pathways. Thalamic neurons integrate spatial information not only within a broader frequency band but also across ITD channels.

FIG. 1

Sound localization pathways in the barn owl. Time (ITD) and intensity (ILD) information are processed in 2 parallel pathways that originate in a bifurcation of the auditory nerve (nVIII) and converge in the inferior colliculus (IC). The IC projects to the forebrain (□) and tectal () sound localization pathways. NM, cochlear nucleus magnocellularis; NA, cochlear nucleus angularis; NL, nucleus laminaris; LLDp, nucleus of the lateral lemniscus pars posterior; ICx, external nucleus of the inferior colliculus; OT, optic tectum; Ov, nucleus ovoidalis; AAr, auditory arcopallium.

FIG. 2

Response properties in Ov and ICx. We located the position of the recording electrodes by the injection of fluorescent tracers. Four different recording sites (seen as white spots) are shown in a photograph of Ov (A) and one recording site in ICx (B). For each neuron we collected ITD-tuning curves (C, F, and I), ILD-tuning curves (D, G, and J) and iso-intensity frequency tuning curves (E, H, and K). Left and middle: curves of Ov neurons shown here correspond to units recorded in the site indicated by * and +, respectively. Right: ICx neuron was recorded in the location marked by tracer injection in B. Error bars represent SE. Scale bar = 1 mm.

FIG. 3

Distribution of best frequencies (BF) in Ov and ICx. A substantial proportion of Ov neurons (■) responded to low frequencies. No BFs <3 kHz were found in ICx ().

FIG. 4

ITD tuning width in Ov and ICx. A: half-width of the main peak of ITD curves collected using broadband noise in Ov (■) and ICx (). The widths were larger in Ov than in ICx. B: width of ITD curve peaks obtained with tones as a function of stimulating frequency (Stim. Freq.). In ICx, widths do not change with frequency (see text). - - - and —, the exponential regression for Ov and ICx data, respectively.

FIG. 5

ITD tuning across frequency in ICx and Ov. Overlaid ITD curves for tones of different frequencies (left) and plots of mean interaural phase (MIP) as a function of stimulating frequency (right), which show a more linear relationship in ICx than in Ov. Each row corresponds to a different unit.

FIG. 6

ITD curves for tonal and narrow band stimulation in Ov. Examples of ITD curves obtained with tones (left) and narrowband stimuli (right). We obtained similar results with both types of acoustic signals. Each row corresponds to a different neuron. The stimulating frequencies (in kHz) are indicated above each plot.