Seasonal variation in avian auditory evoked responses to tones: a comparative analysis of Carolina chickadees, tufted titmice, and white-breasted nuthatches

Abstract

We tested for seasonal plasticity of the peripheral auditory system of three North American members of the Sylvioidea: Carolina chickadees (Poecile carolinensis), tufted titmice (Baeolophus bicolor), and white-breasted nuthatches (Sitta carolinensis). We measured three classes of auditory evoked responses (AER) to tone stimuli: sustained receptor/neural responses to pure-tone condensation waveforms, the frequency-following response (FFR), and the earliest peak of the AER to stimulus onset (tone onset response). Seasonal changes were detected in all classes of AERs in chickadees and nuthatches. Seasonal changes in titmice were restricted to the tone onset response. Interestingly, changes detected in chickadees (and to a lesser extent in titmice) were generally in an opposite direction to changes seen in nuthatches, with chickadees exhibiting greater amplitude AER responses in the spring than in winter, and nuthatches exhibiting greater amplitude AER responses in winter than in spring. In addition, the seasonal differences in the sustained responses tended to be broad-band in the chickadees but restricted to a narrower frequency range in nuthatches. In contrast, seasonal differences in the onset response were over a broader frequency range in titmice than in chickadees and nuthatches. We discuss some possible mechanistic and functional explanations for these seasonal changes.

Vocally correlated seasonal auditory variation in the house sparrow (Passer domesticus)

“…Note, however, that it is unclear whether thresholds under more realistic, noisy conditions vary seasonally, because absolute thresholds do not necessarily predict thresholds in noise (Langemann et al, 1998;Lohr et al, 2003). Previous studies of seasonal auditory plasticity found no variation in thresholds of the plainfin midshipman and northern leopard frog (Sisneros et al, 2004;Goense and Feng, 2005) or in ABR latency of Carolina chickadees, house sparrows and tufted titmice (Lucas et al, 2002;Lucas et al, 2007). White-breasted nuthatches, however, had shorter ABR latency in winter than in spring, suggesting possible seasonal variation in auditory thresholds.…”

“…Single-unit studies of the auditory nerve in plainfin midshipman fish [Porichthys notatus (Sisneros et al, 2004)] and auditory midbrain in northern leopard frogs [Rana pipiens (Goense and Feng, 2005)] showed seasonal variation in the temporal precision of neural responses to the acoustic structure of artificial calls. In songbirds, Lucas and colleagues found preliminary evidence of seasonal variation in auditory brainstem responses (ABRs) of four species, including the house sparrow (Passer domesticus) studied here (Lucas et al, 2002;Lucas et al, 2007). ABRs are voltage waveforms recorded from the scalp that reflect the summed neural onset response of the auditory nerve and brainstem nuclei to sound (Hall, 2007).…”

“…ABRs are voltage waveforms recorded from the scalp that reflect the summed neural onset response of the auditory nerve and brainstem nuclei to sound (Hall, 2007). Responses to clicks and tones were stronger in spring than in winter in Carolina chickadees (Poecile carolinensis) and tufted titmice (Baeolophyus bicolor) and stronger in winter than in spring in white-breasted nuthatches [Sitta carolinensis, a species that sings in winter (Lucas et al, 2002;Lucas et al, 2007)]. In house sparrows, responses to clicks were stronger in spring than in winter (Lucas et al, 2002) but responses to tones were not studied.…”

Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish

“…Mammals show marked decline in auditory sensitivity with age, particularly at higher frequencies within their respective audible ranges (for a review, see Ohlemiller, 2006). Songbirds have been shown to have remarkably stable baseline auditory thresholds throughout ontogeny (Langemann et al, 1999) with species-specific seasonal changes (Lucas et al, 2002;Lucas et al, 2007), whereas studies in fishes have yielded conflicting results (Higgs et al, 2003;Higgs et al, 2002;Iwashita et al, 1999;Kenyon, 1996;Popper, 1971;Sisneros and Bass, 2005). We have investigated peripheral auditory plasticity in a teleost fish, the plainfin midshipman (Porichthys notatus Girard 1854; family Batrachoididae), that shows seasonal, reproductive state-dependent plasticity in the ability to encode the upper harmonics of vocalizations (Fig.1A,B).…”

Steroid Hormones Act Transsynaptically within the Forebrain to Regulate Neuronal Phenotype and Song Stereotypy

“…In seasonally breeding songbirds, there are pronounced hormone-driven seasonal changes in volume and neural morphology of song nuclei, which are accompanied by changes in stereotypy, duration, and production rate of song (Nottebohm, 1981;Ball et al, 2004;Brenowitz, 2004). Only recently have seasonal changes in avian neuronal activity begun to be studied, with research generally focusing on how auditory stimuli are differentially processed (Del Negro and Edeline, 2002;Lucas et al, 2002Lucas et al, , 2007Del Negro et al, 2005) or on how changes in the electrophysiological properties of song nuclei might underlie changes in song behavior (Park et al, 2005;Meitzen et al, 2007).…”