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)