Sound Frequency Representation in the Auditory Cortex of the Common Marmoset Visualized Using Optical Intrinsic Signal Imaging

Abstract

Natural sound is composed of various frequencies. Although the core region of the primate auditory cortex has functionally defined sound frequency preference maps, how the map is organized in the auditory areas of the belt and parabelt regions is not well known. In this study, we investigated the functional organizations of the core, belt, and parabelt regions encompassed by the lateral sulcus and the superior temporal sulcus in the common marmoset (Callithrix jacchus). Using optical intrinsic signal imaging, we obtained evoked responses to band-pass noise stimuli in a range of sound frequencies (0.5-16 kHz) in anesthetized adult animals and visualized the preferred sound frequency map on the cortical surface. We characterized the functionally defined organization using histologically defined brain areas in the same animals. We found tonotopic representation of a set of sound frequencies (low to high) within the primary (A1), rostral (R), and rostrotemporal (RT) areas of the core region. In the belt region, the tonotopic representation existed only in the mediolateral (ML) area. This representation was symmetric with that found in A1 along the border between areas A1 and ML. The functional structure was not very clear in the anterolateral (AL) area. Low frequencies were mainly preferred in the rostrotemplatal (RTL) area, while high frequencies were preferred in the caudolateral (CL) area. There was a portion of the parabelt region that strongly responded to higher sound frequencies (>5.8 kHz) along the border between the rostral parabelt (RPB) and caudal parabelt (CPB) regions.

Keywords: ECoG; histology; marmoset; optical imaging; sound frequency; tonotopy.

Figure 1.

Coronal sections from the left hemisphere of a marmoset stained for myelin and the areal demarcation of the auditory cortical areas. Auditory cortical areas are defined by the myelin structure. The white lines indicate the areal borders. The black filled circles represent positions of blood vessels. The filled and open white arrowheads indicate the lateral sulcus and the superior temporal sulcus, respectively.

Figure 2.

Optical responses to sound frequencies in the auditory cortex of the marmoset shown in Figure 1. A single condition map was reconstructed based on the optical signal changes in response to sound frequencies of 0.5, 0.7, 1, 1.4, 2, 2.9, 4, 5.8, 8, 11.6, and 16 kHz. The response magnitude is indicated by the gray scale shown at the left bottom. The black and white regions indicate the highest and lowest response magnitudes, respectively. The white lines represent the histologically defined areal borders of the auditory cortex.

Figure 3.

Response magnitude maps and the mean response magnitude in each auditory area for the three marmosets. A–C, top, Response magnitude maps reconstructed based on maximum evoked optical signals for sound frequencies of 0.5, 0.7, 1, 1.4, 2, 2.9, 4, 5.8, 8, 11.6, and 16 kHz for each marmoset. The color indicates the maximum signal magnitude at each pixel according to scale bar shown in A. Blood vessel images for each map are shown in the inset. Bottom, The mean response magnitude and SD in each auditory area. LS and STS represent the lateral sulcus and superior temporal sulcus, respectively. D, Time course of optical signals in response to each stimulus frequency in the six regions indicated in A. The colors of the lines correspond to the optical signal evoked for each frequency. The vertical black lines and horizontal red lines represent stimulus onset and the stimulus presentation period, respectively.

Figure 4.

Sound frequency preference maps for the three marmosets. A–C, Sound frequency preference maps reconstructed from averaged responses for all sound frequencies for the three marmosets. The color indicates the preferred frequency at each pixel according to the color code. LS and STS represent the lateral sulcus and superior temporal sulcus, respectively.

Figure 5.

Distribution of preferred sound frequencies in each auditory cortical area. A: relative areas with preference for sound frequencies of 0.5–0.7, 0.7–1, 1–1.4, 1.4–2, 2–2.9, 2.9–4, 4–5.8, 5.8–8, 8–11.6, and 11.6–16 kHz. B, Relative areas with preference for different sound frequencies in the core, belt, and parabelt regions. The pale blue, orange, and gray lines represent the three individual marmosets, and the black line represents the mean value for the three marmosets. The number of asterisks represent the number of animals with significantly biased representation in response to the sound frequency.

Figure 6.

Electrical responses to band-pass noise stimuli. A, ECoG responses to sound frequencies of 1.4, 4, 8, and 16 kHz at four contacts. The horizontal red lines represent the stimulus presentation period. B, left, Electrode positions of the ECoG device on the sound frequency preference map made based on OISI in Figure 4C. Green circles represent the contact positions shown in A. The brown circles correspond to the remaining contacts. LS and STS represent the lateral sulcus and superior temporal sulcus, respectively. Right, Sound frequency preference map reconstructed based on the maximum ECoG responses to all sound frequencies. Color indicates the preferred sound frequency at each contact according to the color code.

Figure 7.

Sound frequency preference map for common marmosets. The circles surrounding H and L indicate regions with preference for high and low frequencies, respectively. The arrows indicate the direction of frequency preference change from low to high. The dotted region represents regions requiring further study. LS and STS represent the lateral sulcus and superior temporal sulcus, respectively. The color map in the simplified schematic of the marmoset cortex in the inset represents the sound frequency preference map.