Habitat-related differences in auditory processing of complex tones and vocal signal properties in four songbirds

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ORIGINAL PAPER

Habitat-related differences in auditory processing of complex tones and vocal signal properties in four songbirds Jeffrey R. Lucas · Alejandro Vélez · Kenneth S. Henry 

Received: 26 September 2014 / Revised: 22 December 2014 / Accepted: 30 January 2015 © Springer-Verlag Berlin Heidelberg 2015

Abstract  We examined temporal processing of harmonic tone complexes in two woodland species (tufted titmice and white-breasted nuthatches) and two open-habitat species (house sparrows and white-crowned sparrows). Envelope and fine-structure processing were quantified using the envelope following response (EFR) and frequency following response (FFR). We predicted stronger EFRs in the open-habitat species based on broader auditory filters and greater amplitude modulation of vocal signals in this group. We predicted stronger FFRs in woodland species based on narrower auditory filters. As predicted, EFR amplitude was generally greatest in the open habitat species. FFR amplitude, in contrast, was greatest in white-crowned sparrows with no clear difference between habitats. This result cannot be fully explained by species differences in audiogram shape and might instead reflect greater acoustic complexity of songs in the white-crowned sparrow. Finally, we observed stronger FFRs in woodland species when tones

were broadcast with the next higher harmonic in the complex. Thus, species such as nuthatches that have songs with strong harmonics may process these sounds using enhanced spectral processing instead of enhanced amplitude-envelope processing. The results suggest coevolution between signal design and temporal processing of complex signals and underscore the need to study auditory processing with a diversity of signals. Keywords  Hearing · Auditory evoked potential · Amplitude envelope · Phase-locking · Audiogram Abbreviations ABR Auditory brainstem response AEP Auditory evoked potential EFR Envelope following response FFR Frequency following rate AM Amplitude modulation

Introduction Electronic supplementary material  The online version of this article (doi:10.1007/s00359-015-0986-7) contains supplementary material, which is available to authorized users. J. R. Lucas (*) · A. Vélez  Department of Biological Sciences, Lilly Hall, Purdue University, 915 W. State St., West Lafayette, IN 47907, USA e-mail: [email protected] Present Address: A. Vélez  Department of Biology, Washington University in St. Louis, St. Louis, MO 63130, USA K. S. Henry  Department of Biomedical Engineering, University of Rochester, 601 Elmwood Ave Box 603, Rochester, NY 14642, USA

Auditory processing mechanisms are expected to evolve in parallel with vocal signals based on the sender–receiver matching hypothesis (Dooling et al. 2000; Gall et al. 2012a). Accordingly, studies on hearing sensitivity across a range of taxa reveal a close match between the frequency range present in conspecific signals and the frequency regions of highest sensitivity in the auditory periphery (e.g., Konishi 1970; Dooling 1982; Szymanski et al. 1999; Sisn