Coding and processing in the auditory systems of FM-signal-producing bats

Abstract

For echolocation, many species of bats emit frequency-modulated (FM) sounds. When the central gray matter or reticular formation in the midbrain is electrically stimulated, these bats produce FM sounds similar to FM-orientation signals. The auditory system is excited by these emitted sounds, but the responses of auditory neurons in the midbrain are attenuated by a neural mechanism operating synchronously with vocalization. This neural attenuating mechanism is present between the auditory nerve and the inferior colliculus and may be a part of mechanisms for effective echo-detection. Among the various orientation sounds emitted by bats, FM sounds are the most suited for echo-ranging. In the lateral lemniscus, the majority of neurons show a very short recovery period, as well as frequent facilitation of their responses to a second tone pulse, so that these neurons are specialized for echo-detection and carry information necessary for echolocation. In the inferior colliculus, single neurons exhibit a broad spectrum of recovery cycles, so that these are probably able to scale echoes from different distances for the distance measurement. Neural-network models of a clock for echo-ranging are discussed. In the inferior colliculus and the auditory cortex, there exist neurons specialized for processing FM signals. For the excitation of these FM-specialized neurons, the direction, range, and speed of frequency sweep are important factors. The FM-specialized neurons always have a large inhibitory area and respond to FM sounds sweeping across this area. Although seemingly paradoxical, such properties are easily explained by neural-network models. Orientation sounds of several species of bats consist of constant frequency (CF) and FM components. Neurons specialized for the analysis of CF sounds have inhibitory areas on both sides of a very narrow excitatory area. The responses of the FM-specialized neurons to certain FM sounds in the presence of either FM or CF sounds are discussed in relation to the inhibitory area.

On the prediction of sweep rate and directional selectivity for FM sounds from two-tone interactions in the inferior colliculus

“…Sideband inhibition model-A number of studies (including this one) have implicated input from an "asymmetrical" inhibitory area (i.e., a single sideband) in the creation of FM directional selectivity. This model is functionally similar to a model of directional selectivity for visual motion discussed by Ruff et al (1987), but was proposed conceptually much earlier to explain FM directionality in the bat auditory system by Suga (1965a) and Suga and Schlegel (1973). In its most parsimonious form, the sideband inhibition model proposes that a directionally selective neuron receives two inputs, one excitatory and the other inhibitory.…”

“…The principle behind the response of this circuit to an FM sweep is simple: sweeps in the preferred direction will elicit more spikes because they stimulate the excitatory area before the inhibitory sideband. By contrast, sweeps in the null-direction elicit fewer spikes, because they activate the inhibitory sideband before the excitatory area, resulting in suppression (akin to forward masking; Fuzessery, 1994;Heil et al, 1992a;Shannon-Hartman et al, 1992;Suga, 1965b;Suga and Schlegel, 1973;Suga et al, 1974).…”

The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats

“…We can only speculate that these cells are selective for other signal types, since FM-and noisespecialized cells have been reported in the IC of bats (e.g. Suga and Schlegel 1973). We could demonstrate that one type of such cells was only driven by binaural stimulation.…”

“…Many aspects of auditory processing at the midbrain level crucially depend on an interplay of excitation and inhibition. In monaural signal analysis, inhibition is involved in shaping temporal response patterns of single units and the form of the excitatory tuning curve in particular at high levels of stimulation, in creating nonmonotonic spike count functions and in producing selectivity for particular frequency-time structures of complex acoustic stimuli (review : Aitkin 1986;Suga 1969;Suga and Schlegel 1973). In binaural signal analysis, excitatory responses evoked by stimulation of one ear are counteracted by inhibition derived from stimulation of the other ear thus producing sensitivity for interaural level or interaural time differences (review: Caird 1991).…”

“…Single unit recordings in the IC have shown that the excitatory tuning curves are flanked by lateral inhibitory sidebands (M611er 1978;Suga 1969;Suga and Schlegel 1973), which can even close the normally V-shaped excitatory area at high stimulus levels (Vater et al 1979;Riibsamen et al 1988;Schmidt et al 1991). The exact arrangement of inhibitory fields governs the neuronal selectivity for pure tones, frequency-modulations (FM) or noise (Suga and Schlegel 1973). Binaural stimulation has revealed a variety of different response types with a predominance of cells excited by the contralateral ear and inhibited by the ipsilateral ear (Schlegel 1977a;Wenstrup et al 1986).…”