Mice and humans perceive multiharmonic communication sounds in the same way

Abstract

Vowels and voiced consonants of human speech and most mammalian vocalizations consist of harmonically structured sounds. The frequency contours of formants in the sounds determine their spectral shape and timbre and carry, in human speech, important phonetic and prosodic information to be communicated. Steadystate partitions of vowels are discriminated and identified mainly on the basis of harmonics or formants having been resolved by the critical-band filters of the auditory system and then grouped together. Speech-analog processing and perception of vowel-like communication sounds in mammalian vocal repertoires has not been demonstrated so far. Here, we synthesize 11 call models and a tape loop with natural wriggling calls of mouse pups and show that house mice perceive this communication call in the same way as we perceive speech vowels: they need the presence of a minimum number of formants (three formants-in this case, at 3.8 ؉ 7.6 ؉ 11.4 kHz), they resolve formants by the critical-band mechanism, group formants together for call identification, perceive the formant structure rather continuously, may detect the missing fundamental of a harmonic complex, and all of these occur in a natural communication situation without any training or behavioral constraints. Thus, wriggling-call perception in mice is comparable with unconditioned vowel discrimination and perception in prelinguistic human infants and points to evolutionary old rules of handling speech sounds in the human auditory system up to the perceptual level.auditory perception ͉ evolution of speech perception ͉ formant filtering and grouping ͉ mouse ͉ sound communication M ouse pups produce so-called wriggling calls when struggling in the nest, mainly when pushing for the teats during suckling by the mother (1). These calls release three types of maternal behavior: namely, licking of pups, changes of suckling position, and nest building, and thus show that they are important communication sounds (2). Wriggling calls usually consist of a fundamental frequency near 4 kHz and several (a minimum of two) overtones reaching to a maximum frequency of about 20 kHz, if overtones within a 30-dB range are considered (Fig. 1). This basic harmonic structure may be modified by frequency modulations of the harmonics and rapid amplitude modulations leading to side bands of the harmonics or to rather noisy partitions of the calls (Fig. 1).Mouse calls are structurally similar to vocalizations of many mammals (3), including cries and other nonverbal sounds of humans, especially infants (4). Because little is known about the perception of these types of vocalizations, we will compare the perceptual properties of wriggling calls with the perception of vowels of human speech that also have a frequency structure similar to that of wriggling calls of mice (5, 6). We hypothesize that mice perceive the wriggling calls in the frequency domain by following the same rules as humans in analyzing, identifying, and grouping formants together to a vowel percept (7-9). The term ''form...

Auditory cortex of bats and primates: managing species-specific calls for social communication

“…We focus here in particular on two species, namely the mustached bat, Pteronotus parnellii, and the rhesus monkey, Macaca mulatta, that have been used for intense studies over the last decade (10)(11)(12)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29). New and interesting findings have also been made in the domestic cat, Felis domestica (16,(30)(31)(32)(33), the house mouse, Mus muscus (34,35), and the marmoset, Callithrix jacchus (36,37) and these contribute to our general perspective of how the mammalian cortex manages complex sounds within the neural domain so as to make the most direct and efficient use of the information present in the acoustic domain. Clearly, each species has the potential to have evolved different strategies that are most appropriate for its environment and sensory requirements.…”

“…Repetition of similar syllables during such vocalization bouts frequently indicates the urgency of a desired response. In mouse pups, wriggling (isolation) calls emitted at high repetition rates and sometimes with increasing amplitudes trigger a retrieval response on the part of maternal females (49,50). This type of sequencing of sounds is less common in animals compared to speech in humans, except in the context of song as in songbirds, bats, dolphins and whales or chorus calls in some species of frogs and primates (51-54).…”

Efficient Encoding Of Vocalizations In The Auditory Midbrain

“…For example, based on the harmonic structure of many species' vocalizations, harmonic combinations of pure tones have been used [Sinex et al, 2002, Ehret, 2002. This greatly reduces the complexity of a multi-tonal stimulus protocol.…”

Distinct Cortical Pathways for Processing Tool versus Animal Sounds

“…However, some of the differential brain activation may have been attributable to differences in the acoustic signal properties (low-level auditory processing) between these two conceptual categories of sound (Nelken et al, 1999;Reide et al, 2001;Ehret and Riecke, 2002;Lewicki, 2002). To explore this possibility, we quantitatively compared (Fig.…”

“…In general, our ability to recognize different types of environmental (nonverbal) sounds is thought to be accomplished, in part, by abstracting the physical properties of a sound and matching them to the known characteristics of a given sound category (Komatsu, 1992;Medin and Coley, 1998). For instance, animal vocalizations often contain frequencies and harmonics that covary in time, which may serve as signal attributes or compound cues for recognition (Nelken et al, 1999;Reide et al, 2001;Ehret and Riecke, 2002). Although less well studied, some sounds produced by tools may share common acoustical features, such as a metallic twang or high-pitched ringing sound, which could conceivably serve as "low-level" signal attributes that aid in our ability to recognize them as tools.…”