1. Orientation sounds (pulses) emitted by the mustached bat (Pteronotus parnellii) consist of up to four harmonics (H-1-4); each harmonic contains a constant frequency (CF) component and a terminal frequency modulated (FM) component, so that there are eight components in total (CF1-4 and FM1-4). By referring the echo from a target to the emitted pulse, the mustached bat derives velocity information from Doppler shift and distance information from echo delay. In this study, the responses of single neurons in the medial geniculate body (MGB) to synthetic biosonar signals were investigated. Stimuli consisted of CF, FM, and CF-FM sounds. Paired CF-FM sounds were used to mimic any two harmonics of pulse-echo pairs. The dorsal and medial divisions of the MGB were found to contain combination-sensitive neurons. These neurons responded poorly to individual sounds regardless of frequency and amplitude and were facilitated by paired sounds presented at particular frequencies, amplitudes, and inter-component intervals (simulated echo delay). Combination-sensitive neurons were tuned to the frequencies that characterize particular components of natural biosonar signals and were classified according to the components of pulse-echo pairs that best matched the spectral selectivity of the neuron. Two classes of combination-sensitive neurons were found, CF/CF and FM-FM. This paper focuses on CF/CF combination-sensitive neurons, which extract velocity information from paired CF components, and on CF2 and CF3 neurons, which, although not combination-sensitive, are tuned to the frequencies of the CF2 and CF3 components of biosonar signals. 2. CF2 and CF3 neurons were sharply tuned in frequency. The best frequencies of the most sharply tuned CF2 neurons were all approximately equal to 61.17 kHz (SD = 370 Hz), which closely matches the frequency at which P. parnellii stabilizes the CF2 component of an echo when compensating for Doppler shift. Thus CF2 neurons are specialized for a fine analysis of Doppler-compensated echoes. 3. Tuning curves of CF2 and CF3 neurons remained narrow regardless of stimulus level. When compared at high stimulus levels (30 and 50 dB above minimum threshold), bandwidths of tuning curves of CF2 and CF3 neurons were much smaller than those of peripheral auditory neurons tuned to CF2 or CF3 frequencies but were about the same as those of cortical neurons tuned to CF2 or CF3 frequencies. Thus the sharpening of neural tuning curves by the bat's central auditory system occurs within or before the MGB. 4. Tuning curves of CF2 and CF3 neurons had inhibitory areas that surrounded and partially overlapped the excitatory areas. Thus CF2 and CF3 neurons were tuned in frequency and amplitude. The neurons that were the most sharply tuned in frequency were also the most sharply tuned in amplitude. These results suggest that the frequency and amplitude selectivity of CF2 and CF3 neurons is increased through lateral inhibition. 5. The signal elements essential to facilitate CF/CF neurons were the CF1 component of the pulse in combination with the CF2 or CF3 component of an echo. 6. CF/CF neurons were tuned to the frequency and amplitude of each component of a paired stimulus. Tuning to CF2 or to CF3 frequencies were very sharp and level tolerant. Tuning to CF1 frequency was sharp in those neurons for which the best facilitative frequency of CF1 was within 700 Hz of the bat's CF1 resting frequency, but relatively broad for the others. Most CF/CF neurons had inhibitory areas adjacent to facilitative areas. 7. The frequency combinations to which most CF/CF neurons were tuned represent small deviations from the exact harmonic relationship such as that found between the CF1 component of pulses emitted by the bat during compensation and the CF2 or CF3 component of Doppler-compensated echoes. When converted to relative velocities, the frequency deviations encoded by most CF/CF neurons corresponded to flight velocities typical of echolocating bats. 8. The response properties of CF/CF neurons recorded in the MGB are qualitatively the same as those of their counterparts in the cortex. The MGB is the lowest nucleus in the ascending auditory pathway known to contain combination-sensitive neurons; combination-sensitive neurons have been sought in the inferior colliculus, but none has been found. Therefore the MGB is likely to be where combination-sensitivity originates. The significance of these results is that the MGB takes an active role in the extraction of biologically important information from complex sound.
