Adaptations of the auditory nervous system for echolocation: Studies of new guinea bats

1. Seven species of paleotropical echolocating bats were studied in an effort to correlate differences in emitted orientation pulses with differences in neural analysis mechanisms. Major emphasis was on species of the genus Hipposideros, which emit extremely high frequencies in pulses consisting of a constant frequency for several msec followed by a fast downward sweep in frequency. 2. Evoked potentials and single unit responses were recorded from the posterior colliculi and more peripheral levels in anesthetized specimens. 3. The emitted orientation sounds of these species are described (Fig. 1, Table 1). Five species (Hipposideros sp. and Aselliscus tricuspidatus) employ similar constant frequency (CW) signals ending in frequency modulation (FM), the main differences being in CW duration and frequency. The two other species (Emballonura niarescens and Pipistrellus papuanus) emit much shorter, essentially purely FM pulses. The orientation pulses of Emballonura are quite unlike those of other emballonurids that have been studied (Table 2). 4. There is a striking correspondence between the frequencies used in emitted pulses and the auditory tuning of each species. As in other bats emitting CW signals, Aselliscus and Hipposideros had prominent “off”-responses to the end of a tone pip. The “off”-potentials were sharply tuned to approximately the frequency of the CW component of the emitted pulses: 58 kc/s in H. diadema, 125–130 kc/s in H. calcaratus, 140–145 kc/s in H. galeritus, and 110–112 kc/s in Aselliscus. Maximal “on”-response sensitivity was at slightly lower frequencies in all species. Only in H. diadema was there significant “on”-response sensitivity at frequencies above that of the maximal “off”-response (Figs. 2, 3). In this respect H. diadema, which emits longer pulses than the other hipposiderids, resembles other species (Rhinolophus ferrum-equinum, Chilonycteris rubiginosa) that emit still longer pulses and have maximal “on”-response sensitivity at frequencies higher than that of the “off”-response. The evoked potentials showed extremely sharp changes in threshold with small changes in frequency. 5. Juvenile specimens of H. galeritus and H. calcaratus emitted sounds of lower frequency than the adults (Fig. 6), and their audiograms were similarly displaced toward lower frequencies (Fig. 3). It is postulated that the range of frequencies emitted may be regulated to correspond to the gradual changes in auditory capabilities as the inner ear matures. 6. Emballonura and Pipistrellus had more broadly tuned responses, with less prominent “off”-responses (Figs. 4, 5). 7. Single units, studied in H. galeritus and Aselliscus, were tuned to the same frequencies as the evoked potentials (Fig. 7). A higher percentage of collicular units responded tonically than are found in bats that emit purely FM pulses. Tuning curves varried greatly in absolute threshold and in sharpness of tuning, with the most narrowly tuned being largely restricted to the highest frequencies (Fig. 8). The dynamic range of most units was only 15–30 db. 8. Collicular single units showed evidence of both inhibitory sharpening of response areas and of multiple excitatory inputs that broadened the response areas (Fig. 9). 9. Several units were studied that responded either at the onset of a tone pip or at its termination, depending on the frequency of the tone pip. These units were consistent with the evoked potentials in showing “off”-responses at the frequency of the emitted CW signal, “on”-responses at just lower frequencies (Fig. 10). 10. With stimuli simulating the bats' own pulses, it was found that the “off” response to the CW component summed with and facilitated response to a terminal FM component. 11. The CW emitting bats showed relatively slow recovery of responsiveness after an initial sound. Response to a following sound did not exceed that to the first at any interval. Recovery was faster at peripheral levels than at the posterior colliculi, and faster at high frequencies than at low (Fig. 11). Single units that showed fast recovery were usually ones that were highly sensitive to stimulus duration (Fig. 12). Emballonura and Pipistrellus recovered more rapidly and showed facilitation of responsiveness at the level of N4 (Fig. 13). 12. Angular sensitivity was studied in the CW producing bats. Greatest sensitivity was typically at 30° to one side and approximately 30° above the plane of the lower jaw (Fig. 14). Some single units were found to be extraordinarily sharply directional, with cut-offs as sharp as 10 db/degree of arc near the midline (Fig. 16). Preceding ipsilateral stimulation was shown to effect sharp, short-term inhibition of excitatory contralateral input (Figs. 17, 18). 13. From response characteristics of the CW-producing bats, it seems probably that the primary function of the CW component in most Hipposideros and Aselliscus is to facilitate responsiveness to the FM sweep. In H. diadema, as in other bats (e.g. Rhinolophus ferrum-equinum and Chilonycteris rubiginosa) that emit longer pulses and have “on”-response sensitivity above the emitted frequency, the CW component is probably also, or primarily, useful for analysis of echo Doppler shift for target detection and localization. 14. It is apparent that mechanisms of auditory information processing may differ sharply in closely related species, and be similar in phylogenetically unrelated species, depending on the types of orientation signals used. Within two families of bats, certain species have been found to emit CW, others FM pulses, and their responses differ accordingly. Emitting largely CW pulses and showing good off responses and slow recovery are the phyllostomatid bat, Chilonycteris rubiginosa, and the emballonurid, Saccopteryx bilineata, while their close relatives Pteronotus suapurensis and Emballonura nigrescens emit mostly FM pulses and respond like vespertilionid bats, with much reduced “off”-responses and fast recovery (see also Grinnell, 1970).