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A Broad Filter Between Call Frequency and Peripheral Auditory Sensitivity Journal of Comparative Physiology A https://doi.org/10.1007/s00359-019-01338-0 ORIGINAL PAPER A broad flter between call frequency and peripheral auditory sensitivity in northern grasshopper mice (Onychomys leucogaster) Dana M. Green1 · Tucker Scolman1 · O’neil W. Guthrie2,3 · Bret Pasch1,3,4 Received: 19 September 2018 / Revised: 18 March 2019 / Accepted: 11 April 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Acoustic communication is a fundamental component of mate and competitor recognition in a variety of taxa and requires animals to detect and diferentiate among acoustic stimuli (Bradbury and Vehrencamp in Principles of animal communication, 2nd edn., Sinauer Associates, Sunderland, 2011). The matched flter hypothesis predicts a correspondence between peripheral auditory tuning of receivers and properties of species-specifc acoustic signals, but few studies have assessed this relation- ship in rodents. We recorded vocalizations and measured auditory brainstem responses (ABRs) in northern grasshopper mice (Onychomys leucogaster), a species that produces long-distance calls to advertise their presence to rivals and potential mates. ABR data indicate the highest sensitivity (28.33 ± 9.07 dB SPL re: 20 μPa) at 10 kHz, roughly corresponding to the fundamental frequency (11.6 ± 0.63 kHz) of long-distance calls produced by conspecifcs. However, the frequency range of peripheral auditory sensitivity was broad (8–24 kHz), indicating the potential to detect both the harmonics of conspecifc calls and vocalizations of sympatric heterospecifcs. Our fndings provide support for the matched flter hypothesis extended to include other ecologically relevant stimuli. Our study contributes important baseline information about the sensory ecol- ogy of a unique rodent to the study of sound perception. Keywords Acoustic communication · Auditory brainstem response · Matched flter · Onychomys Introduction relevant stimuli (Barlow 1961; Wehner 1987). Efcient allocation of sensory resources enhances signal detection The perceptual world of animals emerges from the tuning by maximizing signal-to-noise ratios to facilitate behaviors of nervous systems faced with an excess of external stimuli essential for survival and reproduction (Endler 1993; Lucas (von Uexküll 1934; Wehner 1987; von der Emde and War- et al. 2015). Matched flters for economical sensing (von rant 2016). The matched flter hypothesis proposes that der Emde and Warrant 2016) exist in diverse modalities and sensory systems evolve to detect only the most ecologically taxa, including insect vision and olfaction (Warrant 2016), arachnid mechanoreception (Barth 2016), and fsh electrore- Electronic supplementary material The online version of this ception (von der Emde and Ruhl 2016). article (https ://doi.org/10.1007/s0035 9-019-01338 -0) contains In the acoustic domain, the matched flter hypothesis supplementary material, which is available to authorized users. specifcally predicts a correspondence between peripheral auditory tuning of receivers and properties of species- * Dana M. Green [email protected] specifc acoustic signals (Capranica and Mofat 1983). In crickets and anurans, matching of the peripheral auditory 1 Department of Biological Sciences, Northern Arizona system with the dominant frequency of male advertise- University, 617 S. Beaver Street, Flagstaf, AZ 86011, USA ment signals facilitates discrimination of conspecifcs 2 Cell and Molecular Pathology Laboratory, Department from heterospecifcs (Gerhardt and Schwarz 2001; Ger- of Communication Sciences and Disorder, Northern Arizona hardt and Huber 2002). Similarly, many birds exhibit University, Flagstaf, AZ 86011, USA heightened peripheral auditory tuning for species-specifc 3 Center for Bioengineering Innovation, Northern Arizona frequency and temporal parameters to facilitate social University, Flagstaf, AZ 86011, USA communication (Dooling et al. 1979; Gall et al. 2012). 4 Merriam-Powell Center for Environmental Research, The relationship between peripheral auditory tuning and Northern Arizona University, Flagstaf, AZ 86011, USA Vol.:(0123456789)1 3 Journal of Comparative Physiology A species-specifc vocalizations is less well described in identify whether the peripheral auditory fltering applies mammals in part due to a focus on selective encoding of more broadly across diferent taxa and contexts. acoustic stimuli in the central auditory pathway that inte- Northern grasshopper mice (Onychomys leucogaster) grates inputs from the brainstem, the auditory cortex, and are cricetid rodents of western North America that feed on associated cortical areas (Holmstrom et al. 2010; Portfors arthropods and small vertebrates (Bailey and Sperry 1929; and Roberts 2014; Portfors 2018). However, recent evi- Flake 1973). As a consequence of their predatory lifestyle, dence in rodents suggests that subcortical auditory nuclei grasshopper mice have large home ranges (1.72 ± 0.68 ha; play an important role in mediating behavioral responses Stapp 1999) for their body size (McNab 1963). Like other to ecologically relevant sounds (Portfors 2018). For exam- muroid rodents, grasshopper mice produce USVs (~ 50 kHz) ple, pup rearing experience shortens maternal auditory in close-distance mating contexts (Miller and Engstrom brainstem response latencies to promote recognition of 2012; Pasch et al. 2017). However, the genus is unique infant isolation vocalizations (Miranda et al. 2014). Such among mice in their ability to produce audible long-distance fndings have contributed to increased interest in the role advertisement vocalizations to announce their presence to of the peripheral auditory system to rodent sound percep- potential mates and competitors (Rufer 1966; Frank 1989). tion in ecologically relevant contexts (Kubke and Wild As females enter receptivity during the summer mating sea- 2018; Portfors 2018). son, both males and females call reciprocally to facilitate Although many rodents produce both sonic and ultra- localization (Frank 1989). Long-distance calls consist of a sonic vocalizations (USV) to mediate social interactions fundamental frequency (F0) and a series of harmonic over- (Kalcounis-Rueppell et al. 2006; Portfors 2007; Briggs tones at integer multiples of F0 (Pasch et al. 2017; Fig. 1), and Kalcounis-Rueppell 2011; Hanson and Hurley 2012), with populations varying in both call F0 (9.5–13.5 kHz) and laboratory mice and rats account for most studies of hear- the degree of sexual dimorphism (Hafner and Hafner 1979; ing physiology (Dent et al. 2018). In addition, such studies Miller and Engstrom 2012; Pasch et al. 2016). In southwest- often occur in the context of biomedical applications and ern New Mexico, the species is sympatric with two smaller are largely divorced from ethologically relevant acoustic congeners (Chihuahuan grasshopper mice, O. arenicola, and signals that mediate social behavior (Bennur et al. 2013). southern grasshopper mice, O. torridus) that produce higher The comparatively few studies of auditory sensitivity in frequency species-specifc calls (Pasch et al. 2016). exotic rodents are based on behavioral audiograms (e.g., Despite their unique mode of acoustic communication, Webster and Webster 1972; Hefner 1980; Hefner and only two studies have explored auditory sensitivity in grass- Hefner 1985, 1990, 1992) and/or did not relate auditory hopper mice. Conditioned avoidance procedures indicate sensitivity to the vocal repertoire of the species (Ralls that northern grasshopper mice (n = 3) from western Kan- 1967; Katbamna et al. 1996; Zhou et al. 2006). Broadly, sas are most sensitive to 8 kHz tones (Hefner and Hefner studies are lacking that relate hearing physiology to vocali- 1985) and have an enhanced ability to localize sound rela- zations in non-model rodents, thus limiting our ability to tive to other rodents (Hefner and Hefner 1988). However, no studies have simultaneously quantifed call characters acb F0 50 0 4F0 -10 40 2F 3F 0 0 -20 ) 30 -30 2F0 3F0 -40 20 Frequency (kHz 4F Relative amplitude (dB) -50 0 F0 10 -60 0 0.5 1 1.5 0 10 20 30 40 50 Time (s) Frequency (kHz) Fig. 1 Long-distance vocalization of a northern grasshopper mice. a F0 fundamental frequency, 2F0 2nd harmonic, 3F0 3rd harmonic, An illustration of a mouse calling, b spectrogram and c power spec- 4F0 4th harmonic. Harmonics are integer multiples of F0 trum of a long-distance vocalization from a male recorded at 33.3 cm. 1 3 Journal of Comparative Physiology A and auditory tuning to explore the degree to which vocali- calls recorded (x ̄= 38.3, range = 1–250). Values are reported zations are matched to their peripheral auditory sensitiv- as ± standard deviation. ity. In this study, we quantifed the F0 of long-distance vocalizations and hearing thresholds of northern grasshop- Auditory‑evoked potentials per mice from southwestern New Mexico using auditory brainstem responses (ABR; Willott 2006). ABRs are a To estimate auditory-evoked potentials, we tested separate relatively non-invasive method to record auditory-evoked captive bred ofspring of wild-captured mice (n = 18, 9/sex) potentials of the cochlear ganglion neurons and nuclei of between the ages of 6–18 month in a shielded semi-ane- the central auditory pathway from electrodes on the scalp choic chamber (ETS Lindgren SD-1; internal dimensions (Hall 2007). We focused on frequencies (4–32 kHz) sur- 91.4 cm × 91.4 cm × 91.4 cm) lined with acoustic foam. rounding those reported for long-distance vocalizations of O. Following measurement of mass, we administered
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