Temporal Coding of Concurrent Acoustic Signals in Auditory Midbrain

Abstract

A fundamental problem faced by the auditory system of humans and other vertebrates is the segregation of concurrent vocal signals. To discriminate between individual vocalizations, the auditory system must extract information about each signal from the single temporal waveform that results from the summation of the simultaneous acoustic signals. Here, we present the first report of midbrain coding of simultaneous acoustic signals in a vocal species, the plainfin midshipman fish, that routinely encounters concurrent vocalizations. During the breeding season, nesting males congregate and produce longduration, multiharmonic mate calls that overlap, producing beat waveforms. Neurophysiological responses to two simultaneous tones near the fundamental frequencies of natural calls reveal that midbrain units temporally code the difference frequency (dF). Many neurons are tuned to a specific dF; their selectivity overlaps the range of dFs for naturally occurring acoustic beats.Beats and amplitude-modulated (AM) signals are also coded differently by most units. Although some neurons exhibit differential tuning for beat dFs and the modulation frequencies (modFs) of AM signals, others exhibit similar temporal selectivity but differ in their degree of synchronization to dFs and modFs. The extraction of dF information, together with other auditory cues, could enable the detection and segregation of concurrent vocalizations, whereas differential responses to beats and AM signals could permit discrimination of beats from other AM-like signals produced by midshipman. A central code of beat dFs may be a general vertebrate mechanism used for coding concurrent acoustic signals, including human vowels.

Novel underwater soundscape: acoustic repertoire of plainfin midshipman fish

“…10E), and overlapping hums or beats (Fig. 10F) produced by nearby males (see Bass et al, 1999;Bodnar and Bass, 1997). Growl AM showed instability ( Fig.…”

The representation of conspecific sounds in the auditory brainstem of teleost fishes

“…For other purposes, such as investigating critical bandwidths (Tavolga, 1974;Hawkins and Chapman, 1975), masking effects (Buerkle, 1969;Fay, 1974;Fay and Coombs, 1988) or other aspects of auditory processing in fishes, more complex sound stimuli were used. Such sinusoidal amplitude-modulated tones, noise bands, beats or click trains sometimes approached the characteristics of natural sounds (Bodnar and Bass, 1997;McKibben and Bass, 1998;Marvit and Crawford, 2000). The sound stimuli used in fish audiology, however, often did not reflect sounds that the animals actually confronted in their environment.…”

“…This may be induced by a different activation pattern in the neurons and indicates that the perception of differences probably also relies on other characteristics such as pulse duration or envelope shape of the stimulus. There is evidence that in plainfin midshipman the different frequency of acoustic beats and the modulation frequency of amplitude-modulated signals are coded differently by neurons in the auditory midbrain, even if it is the same frequency (Bodnar and Bass, 1997). This could permit discrimination of beats (due to concurrent vocalizations of males during the breeding season) from other amplitudemodulated like signals.…”

Novel vocal repertoire and paired swimbladders of the three-spined toadfish,Batrachomoeus trispinosus: insights into the diversity of the Batrachoididae

“…Single neuron recording studies of the auditory system of batrachoidids also show the temporal encoding of two-tone beat stimuli. For midshipman, sensitivity to stimuli with 1-10 Hz beat frequencies overlaps that of the naturally occurring beats generated by the concurrent humming of neighboring males during the breeding season (Bodnar and Bass, 1997). The auditory system of the toadfish O. beta also encodes beats, but mainly for beat frequencies >10 Hz .…”