1. Delay-tuned combination-sensitive neurons (FM-FM neurons) have been discovered in the dorsal and medial divisions of the medial geniculate body (MGB) of the mustached bat (Pteronotus parnellii). In this paper we present evidence for a thalamic origin for FM-FM neurons. Our examination of the response properties of FM-FM neurons indicates that the neural mechanism of delay-tuning depends on coincidence detection and involves an interaction between neural inhibition and excitation. 2. The biosonar pulse (P) and its echo (E) produced and heard by the mustached bat consist of four harmonics; each harmonic contains a constant frequency (CF) component and a frequency modulated (FM) component. Thus the pulse-echo pair contains eight CF components (PCF1-4, ECF1-4) and eight FM components (PFM1-4, EFM1-4). The stimuli used in this study consisted of CF, FM, and CF-FM sounds: paired CF-FM sounds were used to simulate any two harmonics of pulse-echo pairs. The responses of FM-FM neurons in the MGB were recorded extracellularly. We found that FM-FM neurons respond poorly or not at all to single sounds, respond strongly to paired sounds, and are tuned to the frequency and amplitude of each sound of the pair and to the time interval separating them (simulated echo delay). 3. All FM-FM neurons are facilitated by paired FM sounds and most are facilitated by paired CF sounds. Best facilitative frequencies measured with paired CF sounds fall outside the frequency ranges of the CF components of biosonar signals, whereas best facilitative frequencies measured with paired FM sounds fall within the frequency ranges of the FM components of biosonar signals. Thus FM-FM neurons are expected to respond selectively to combinations of FM components in biosonar signals. The FM components of pulse-echo pairs essential to facilitate FM-FM neurons are the FM component of the fundamental of the pulse (PFM1) in combination with the FM component of the second, third, or fourth harmonic of an echo (EFM2, EFM3, EFM4; collectively, EFMn). 4. The frequency combinations to which FM-FM neurons are tuned reflect small deviations from the harmonic relationship such as occurs in combinations of FM components from pulses and Doppler-shifted echoes. Compared with CF/CF neurons, however, FM-FM neurons are broadly tuned to stimulus frequency. Thus FM-FM neurons are Doppler-shift tolerant and relatively unspecialized for processing velocity information in the frequency domain.(ABSTRACT TRUNCATED AT 400 WORDS)
1. The auditory midbrain in Eptesicus contains delay-tuned neurons that encode target range. Most delay-tuned neurons respond poorly to tones or individual frequency-modulated (FM) sweeps and require combinations of FM sweeps. They are combination sensitive and delay tuned. The index of facilitation (IF), a coefficient measuring combination sensitivity for individual delay-tuned neurons, ranged from 0.14 to 1.0, with an average of 0.64 +/- 0.24 (mean +/- SD). Of the 33 facilitated responses from 29 neurons, 23 (70%) exhibited IFs > 0.5, which corresponds to a facilitated response 3 times greater than the sum of the responses to individual pulse and echoes. Thus the responses of midbrain delay-tuned neurons are highly combination sensitive. 2. The response of midbrain delay-tuned neurons is phasic, with an average of 0.7 +/- 0.4 action potentials elicited per optimal pulse-echo pair. Thus midbrain delay-tuned neurons in Eptesicus act as probability encoders. 3. The distribution of best echo delays (BDs) of midbrain delay-tuned neurons ranged from 8 to 30 ms. As an ensemble, midbrain delay-tuned neurons encode target ranges of 138-516 cm. There is a basic correspondence between the physiologically determined span of midbrain BDs between 8 and 30 ms and the behaviorally determined borders of the approach (8- to 17-ms echo delay) and search stages (17- to 30-ms echo delay) of the insect pursuit sequence. Midbrain delay-tuned neurons can be separated into two subpopulations on the basis of the difference in distributions of the echo best amplitude (EBA) tuning at BD. The BDs of one subpopulation correspond to the span of search stage echo delays, and the BDs of the other subpopulation correspond to the span of approach stage echo delays. 4. EBAs of neurons in each subpopulation are tailored to the specific perceptual requirements of the corresponding behavioral stage. EBAs of midbrain neurons tuned to echo delays between 17 and 30 ms (N = 12) correspond to the search stage and are suited to the requirements of target detection. EBAs of midbrain neurons tuned to echo delays between 17 and 30 ms (N = 21) correspond to the approach stage and are suited to the requirements of target size discrimination. 5. The best FM sweeps for the pulse (PFM) and echo (EFM) were determined for each midbrain neuron. PFMs appear to cluster at frequencies corresponding to the three harmonic peaks in the emitted pulse power spectra.(ABSTRACT TRUNCATED AT 400 WORDS)
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