Songbird frequency selectivity and temporal resolution vary with sex and season

Proceedings of the Royal Society B: Biological Sciences, Jan 2013

Many species of songbirds exhibit dramatic seasonal variation in song output. Recent evidence suggests that seasonal changes in auditory processing are coincident with seasonal variation in vocal output. Here, we show, for the first time, that frequency selectivity and temporal resolution of the songbird auditory periphery change seasonally and in a sex-specific manner. Male and female house sparrows (Passer domesticus) did not differ in their frequency sensitivity during the non-breeding season, nor did they differ in their temporal resolution. By contrast, female house sparrows showed enhanced frequency selectivity during the breeding season, which was matched by a concomitant reduction of temporal resolution. However, males failed to show seasonal plasticity in either of these auditory properties. We discuss potential mechanisms generating these seasonal patterns and the implications of sex-specific seasonal changes in auditory processing for vocal communication.

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

https://rspb.royalsocietypublishing.org/content/280/1751/20122296.full.pdf

Songbird frequency selectivity and temporal resolution vary with sex and season

Author for correspondence: Megan D. Gall e-mail: mgall 1 @gsu.edu Megan D. Gall 1 Therese S. Salameh 0 Jeffrey R. Lucas 0 0 Department of Biological Sciences, Purdue University , 915 W. State Street, West Lafayette, IN 47907 , USA 1 Neuroscience Institute, Georgia State University , 100 Piedmont Avenue SE, Atlanta, GA 30303 , USA Many species of songbirds exhibit dramatic seasonal variation in song output. Recent evidence suggests that seasonal changes in auditory processing are coincident with seasonal variation in vocal output. Here, we show, for the first time, that frequency selectivity and temporal resolution of the songbird auditory periphery change seasonally and in a sex-specific manner. Male and female house sparrows (Passer domesticus) did not differ in their frequency sensitivity during the non-breeding season, nor did they differ in their temporal resolution. By contrast, female house sparrows showed enhanced frequency selectivity during the breeding season, which was matched by a concomitant reduction of temporal resolution. However, males failed to show seasonal plasticity in either of these auditory properties. We discuss potential mechanisms generating these seasonal patterns and the implications of sex-specific seasonal changes in auditory processing for vocal communication. 1. Introduction The behavioural salience of mate attraction and courtship signals changes seasonally in many songbird species [1]. Recent evidence suggests that plasticity in neural sensory representation may play an important role in generating this variation in the behavioural salience of song [2 5]. For instance, female white-throated sparrows (Zonotrichia albicollis) in breeding condition show differential neural responses, as measured with immediate early gene activity, to conspecific song versus tones [5]. These same females will also produce a behavioural response (copulation solicitation display) in response to playback of male song [5]. However, females that are not in breeding condition do not show differential neural responses to conspecific songs and tones, and playback of the male song does not induce the behavioural response of a copulation solicitation display [5]. The neural representation of sound begins at the auditory periphery. Yet, we know substantially less about seasonal changes in peripheral auditory processing in songbirds, compared with central auditory processing. However, recent evidence suggests that plasticity in sensory processing correlated with reproduction may begin at the periphery [6 9]. Because peripheral auditory filters gate information travelling to the central auditory system, they are expected to play an important role in determining the salience of spectral and temporal vocal features. The peripheral auditory filters are especially important in the resolution of an important trade-off between frequency resolution and temporal resolution [10,11]. This trade-off is known as the uncertainty principle (see [12] for an application to the analysis of birdsong). This trade-off arises because auditory filters that integrate a signal over a long period of time provide enhanced frequency resolution [10]. However, patterns in the temporal domain can be lost when the integration time of an auditory filter is long [11]. The anatomical resolution of the trade-off between timing and frequency information is determined in part by the bandwidth of the auditory filter [10,11]. Auditory filters with narrow bandwidths tend to have longer integration times and generally enhance frequency resolution, while broad bandwidth auditory filters have short integration times and enhance temporal resolution. Thus, if the bandwidth of the auditory filters changes seasonally, the information being passed to the central auditory system will probably alter the representation of vocal signals in the central auditory system. Here, we investigated sex and seasonal variation in house sparrow auditory filters and temporal resolution. Females show a seasonal change in their response to male vocalizations [13,14]. Therefore, we predicted that female house sparrows would show seasonal plasticity in the bandwidth of their auditory filters and, concomitantly, temporal resolution. Currently, little is known about the vocal features that elicit female sexual response in house sparrows; therefore, we could not predict the direction of change (i.e. whether auditory filters would increase or decrease in bandwidth, or whether temporal resolution would be diminished or improved). Additionally, we predicted that males and females would differ in their auditory processing during the breeding season. During the non-breeding season, males and females show behavioural responses similar to conspecific vocalizations [13,14]. Therefore, we predicted that during the non-breeding season, males and females would not differ in their auditory processing. 2. Methods (a) Capture, housing and experimental design All breeding season in (...truncated)


This is a preview of a remote PDF: https://rspb.royalsocietypublishing.org/content/280/1751/20122296.full.pdf

Megan D. Gall, Therese S. Salameh, Jeffrey R. Lucas. Songbird frequency selectivity and temporal resolution vary with sex and season, Proceedings of the Royal Society B: Biological Sciences, 2013, 280/1751, DOI: 10.1098/rspb.2012.2296