Spatial organization of frequency preference and selectivity in the human inferior colliculus

Abstract

To date, the functional organization of human auditory subcortical structures can only be inferred from animal models. Here we use high-resolution functional magnetic resonance imaging at ultra-high magnetic fields (7T) to map the organization of spectral responses in the human inferior colliculus, a subcortical structure fundamental for sound processing. We reveal a tonotopic map with a spatial gradient of preferred frequencies approximately oriented from dorsolateral (low frequencies) to ventromedial (high frequencies) locations. Furthermore, we observe a spatial organization of spectral selectivity (tuning) of functional magnetic resonance imaging responses in the human inferior colliculus. Along isofrequency contours, functional magnetic resonance imaging tuning is narrowest in central locations and broadest in the surrounding regions. Finally, by comparing subcortical and cortical auditory areas we show that functional magnetic resonance imaging tuning is narrower in human inferior colliculus than on the cortical surface. Our findings pave the way to noninvasive investigations of sound processing in human subcortical nuclei and for studying the interplay between subcortical and cortical neuronal populations.

Figure 1. Tonotopic maps in the hIC based on Experiments 1 and 2

Maps of frequency preference (tonotopic maps) in the inferior colliculus (IC) for a representative subject (a) and in the group (b) obtained from single tones (three main frequencies, Experiment 1) and natural sounds (Experiment 2). Sagittal (left panel) and coronal (right panel) views of the maps are superimposed on high resolution anatomical images of the subject (a) and to the anatomical images obtained from the average of all subjects (b). The red arrow in the sagittal sections indicates the dorsal (D) to ventral (V) direction in the human IC.

Figure 2. Tonotopic maps in the hIC based on Experiment 2

Maps of frequency preference (tonotopic maps) in the inferior colliculus (IC) for a representative subject (a) and in the group (b) obtained from single tones (eight center frequencies, Experiment 3). Sagittal and coronal views of the maps are superimposed on high resolution anatomical images of the subject (a) and to the anatomical images obtained from the average of all subjects (b). The red arrow in the sagittal sections indicates the dorsal (D) to ventral (V) direction in the human IC.

Figure 3. Frequency gradient in the human inferior colliculus

Direction of the frequency gradient in the left and right human inferior colliculus as obtained from the response to simple tones (Experiment 1). Angles are referred to a vector pointing in the anterior to posterior directions as indicated in the figure. Gray arrows indicate single subject results, and colored arrows indicated results obtained from the group tonotopic maps. The dorsal (D) to ventral (V) direction in the human IC is indicated by a black dotted line.

Figure 4. Tuning width maps in the human inferior colliculus

Eight equally spaced sagittal slices (four in the left IC and four in the right IC) of the group tonotopic map (red-yellow-green-blue scale), as obtained in Experiment 1 (‘tones’) superimposed to group-averaged anatomical images (a). Group tuning width map (purple-blue-green-yellow scale), as obtained in Experiment 2 (‘natural sounds’) (b). The map is superimposed to group-averaged anatomical images for the same eight equally spaced sagittal slices presented in (a). Spectral tuning sampled along the 1.5 kHz iso-frequency line for the same eight equally spaced slices presented in (a–b) (dashed line marks the center of the iso-frequency line) (c). Averaged distribution (mean and standard deviation across slices) of spectral tuning along the 1.5 kHz iso-frequency line (d). The dashed line marks the center of the iso-frequency line.

Figure 5. Tuning width distribution in the human inferior colliculus and cortex

Histograms of voxels’ tuning width (BF in Hz/FWHM in Hz) for each region (inferior colliculus – gray, hA1 – red, hR – green, lateral belt – blue) and hemisphere. Note that a larger proportion of narrowly tuned voxels are present in hIC (gray curves; high values), while lateral belt regions contain a larger proportion of broadly tuned voxels (blue curves; low values).

Figure 6. Comparison of tuning width distributions of different auditory stages

The percentage of voxels with spectral tuning (BF/FWHM) within four different windows ([0 – 0.82], [0.82 – 1.63], [1.63 – 2.52], [2.52 – 3.23]) is reported for four different areas (inferior colliculus – gray, hA1 – red, hR – green, lateral belt – blue) in both left (left column) and right (right column) hemispheres. Error bars represent standard deviations across subjects. Dashed lines mark significant differences (Wilcoxon ranksum test; p = 0.05; n = 5).