Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of target range information

Abstract

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)

Spatially Selective Auditory Responses in the Superior Colliculus of the Echolocating Bat

“…In contrast to the sharply delay-tuned responses observed in the MGB (Olsen and Suga, 1991) and AC of the mustache bat (Suga and Horikawa, 1986), delay-facilitated neurons in SC and other structures of Eptesicus (DNLL: Covey, 1993;ITN: Dear and Suga, 1995;AC: Dear et al, 1993a) are broadly tuned along the range axis. In the mustache bat, thalamic and cortical delay-sensitive neurons respond predominantly to delay values corresponding to close target ranges, typically between 14 and 140 cm, although BDs for ranges up to 400 cm also were reported (Suga and Horikawa, 1986).…”

“…Echo-delay facilitation has been demonstrated previously in several species of bat and in several structures of the ascending auditory pathway, including dorsal nucleus of the lateral lemniscus (DNLL) (Covey, 1993), intertectal nucleus (ITN) (Feng et al, 1978;Dear and Suga, 1995), inferior colliculus (IC) (Mittmann and Wenstrup, 1994;Yan and Suga, 1996), medial geniculate body (MGB) (Olsen and Suga, 1991), and auditory cortex (AC) (Suga and O'Neill, 1979;Wong and Shannon, 1988;Dear et al, 1993a,b). Comparing the mean neural response latencies across structures studied in Eptesicus fuscus, the time to firing in the SC (2D: 8.5 Ϯ 3.4 msec; 3D: 9.7 Ϯ 2.3 msec) falls between the average latencies reported for DNLL (7.8 Ϯ 3.5 msec; Covey, 1993) and AC (non-delay-tuned: 13.8 Ϯ 5.7 msec; delay-tuned: 12.1 Ϯ 5.5 msec, Dear et al, 1993b), although the overlap with the brainstem nucleus is considerable.…”

“…3B) (Dear et al, 1993b). For the special case of echo-delay facilitation, the magnitude of facilitation was quantified as a ratio or index of facilitation with respect to the sum of responses to each stimulus element (Olsen and Suga, 1991;Dear and Suga, 1995)…”

Temporal Masking Reveals Properties of Sound-Evoked Inhibition in Duration-Tuned Neurons of the Inferior Colliculus

“…For example, if the response of a delay-tuned neuron in the auditory thalamus (Olsen and Suga, 1991) depended on coincidence of inputs from duration-tuned neurons, then it would detect the delay of two sounds with specific durations. Because duration-tuned neurons are also tuned to frequency and, in some cases, signal amplitude, these variables add additional dimensions to their response specificity.…”

Echo-acoustic flow dynamically modifies the cortical map of target range in bats

“…Echolocating bats use the delay between their sonar calls and the reflected echoes to measure target range, a parameter of crucial importance for avoiding collisions or capturing prey 8,9 . Neurons at different stages of the ascending auditory pathway have been shown to selectively encode specific call/echo delays in their response rate [10][11][12] . This echo delay selectivity has been shown to emerge in the midbrain, and is then reorganized in the dorsal auditory cortex to represent target range in an orderly organized map 13 .…”