Functional organization of mustached bat inferior colliculus: I. Representation of FM frequency bands important for target ranging revealed by 14C‐2‐deoxyglucose autoradiography and single unit mapping

Abstract

The representation in the inferior colliculus of the frequency modulated (FM) components of the first (25–30 kHz) and second (50–60 kHz) harmonic of the sonar signal of the mustached bat, which may be important for target range processing, was investigated by using the 2‐deoxyglucose (2‐DG) technique and single‐unit mapping. In the 2‐DG experiments, bats presented with second harmonic FM stimuli alone showed uptake of label in specific regions of the central nucleus and dorsal cortex of the inferior colliculus, and the nucleus of the brachium. In the central nucleus, a dorsoventrally and mediolaterally elongated slab at the caudal border of the anterolateral division was observed. Labeling in the dorsal cortex was contiguous with this band. Bats stimulated with pairs of first and second harmonic FM stimuli separated by short time delays showed similar patterns of labeling, with the addition of another dorsoventrally elongated region of uptake in the more rostral part of the anterolateral division, associated with label in the dorsal cortex. By comparison to control cases exposed to delayed pairs of first and third harmonic signals, or to a second harmonic constant‐frequency tone burst at the bat's reference frequency (ca. 60 kHz), we deduced that this additional region of uptake was attributable to the first harmonic FM component. To elucidate further the details of the tonotopic organization and to correlate the frequency representation with anatomical features of the IC, finegrained maps of single‐unit best frequencies were obtained in the central nucleus. Isofrequency contours were reconstructed by computer from five bats after focal, iontophoretic injection of horseradish peroxidase to locate the penetrations and trace connections of the FM₂ area. We found that the tissue volume representing FM₂ frequencies (50‐60 kHz) showed approximately a sixfold overrepresentation for this frequency band. This region occupied most of the caudal portion of the anterolateral division of the central nucleus. Only a single tonotopic representation was found in the central nucleus, consistent with the pattern seen in other mammals. However, isofrequency contours in the anterolateral division were oriented dorsoventrally, approximately parallel to the coronal plane. The small band of frequencies (ca. 60–62 kHz) associated with the dominant con‐ stant‐frequency component of the biosonar signal was even more dramatically overrepresented (40×) and was confined to the dorsoposterior division, as pre‐ viously reported by Zook et al. (1985, 530–456). The first‐harmonic FM fre‐ quencies (25–30 kHz) were localized rostrolaterally in the anterolateral division, confirming our 2‐deoxyglucose experiments. Frequencies above 65 kHz were found only in the medial division, where the isofrequency contours were also vertically oriented. The disproportionate representation of the FM2 band correlates well with its importance both as a cue for target ranging and as a critical acoustic element for the excitation of delay‐dependent “FM‐FM” facilitation neurons found at the thalamic and cortical levels of the mustached bat auditory system.