He hears, she hears: are there sex differences in auditory processing?

Abstract

Songbirds learn individually unique songs through vocal imitation and use them in courtship and territorial displays. Previous work has identified a forebrain auditory area, the caudomedial nidopallium (NCM), that appears specialized for discriminating and remembering conspecific vocalizations. In zebra finches (ZFs), only males produce learned vocalizations, but both sexes process these and other signals. This study assessed sex differences in auditory processing by recording extracellular multiunit activity at multiple sites within NCM. Juvenile female ZFs (n = 46) were reared in individual isolation and artificially tutored with song. In adulthood, songs were played back to assess auditory responses, stimulus-specific adaptation, neural bias for conspecific song, and memory for the tutor's song, as well as recently heard songs. In a subset of females (n = 36), estradiol (E2) levels were manipulated to test the contribution of E2, known to be synthesized in the brain, to auditory responses. Untreated females (n = 10) showed significant differences in response magnitude and stimulus-specific adaptation compared to males reared in the same paradigm (n = 9). In hormone-manipulated females, E2 augmentation facilitated the memory for recently heard songs in adulthood, but neither E2 augmentation (n = 15) nor E2 synthesis blockade (n = 9) affected tutor song memory or the neural bias for conspecific song. The results demonstrate subtle sex differences in processing communication signals, and show that E2 levels in female songbirds can affect the memory for songs of potential suitors, thus contributing to the process of mate selection. The results also have potential relevance to clinical interventions that manipulate E2 in human patients.

Keywords: estradiol; learning; memory; sex differences; zebra finch.

Figure 1

Experimental timeline. Juvenile female zebra finches (n=46) were exposed to adult male song from d45 to d85. In adulthood, a subset of these females received no further treatment and underwent electrophysiological testing (n=10) in order to assess sex differences in response to song. The remainder (n=36) received hormonal manipulations that began 9 days prior to electrophysiological testing in order to assess the effects of estradiol on song memory. Auditory stimuli included the tutor song and novel and familiar conspecific and heterospecific songs.

Figure 2

A) Representative responses at 3 recording sites in NCM. Raw multi-unit records (green and black traces) are shown for a single trial. To calculate the response amplitude at a given site, the response during the Control (C) window (black box; 500ms of silence prior to stimulus onset) was subtracted from the response during the Response (R) window (red box; stimulus presentation + 100ms of silence). R-C was calculated for each trial of each stimulus for each recording site. B) The response magnitude of multiunit activity recorded at one site in NCM during presentation of four songs that were previously heard during training (T1, T2) or were novel (N1, N2). Songs were played 25 times each in shuffled order, but responses have been reordered for clarity. Adaptation rates were calculated for trials 6–25 (gray lines) and are shown at the top of each panel.

Figure 3

Sex differences in NCM responses to novel zebra finch songs. A) Recordings in females (F) had lower response magnitudes than in males (M). B) Recordings in females had shallower adaptation rates than in males.

Figure 4

Familiarity indices (FIs) for the Tutor Song did not differ significantly between tutored females (F) and tutored males (M). FI is calculated as the average adaptation rate to novel songs/average adaptation rate to Tutor song. When FI = 1 (dashed line), adaptation rates are equal, indicating no familiarity for the Tutor song.

Figure 5

Familiarity indices (FIs) for songs heard 6h prior to NCM recording in adults. FIs for the recently heard songs indicated familiarity that did not differ between females (F) and males (M). When FI = 1 (dashed line), adaptation rates are equal, indicating no familiarity for the training songs.

Figure 6

Tutor song memory is not affected by hormone treatment. FIs to the tutor-song indicated familiarity that did not differ significantly among females that were treated with Fadrozole (FAD), Estradiol (E2), or Saline (SAL). When FI = 1 (dashed line), adaptation rates are equal, indicating no familiarity for the training songs.

Figure 7

Effects of hormone treatment on FIs for songs heard 6h earlier in adult females. FIs for the training songs heard 6 hours prior to NCM recording were significantly greater in estradiol-treated (E2) than in Fadrozole (FAD) or saline-treated (SAL) females. FIs were unexpectedly low in SAL birds (cf. Figure 5 for untreated females).

Figure 8

Responses to conspecific and heterospecific song. Response magnitudes were significantly higher to novel conspecific (solid bars, zebra finch) than to novel heterospecific (open bars, canary) songs in all treatment groups (FAD, Fadrozole; SAL, saline; E2, estradiol).