Sex differences in the representation of call stimuli in a songbird secondary auditory area

Abstract

Understanding how communication sounds are encoded in the central auditory system is critical to deciphering the neural bases of acoustic communication. Songbirds use learned or unlearned vocalizations in a variety of social interactions. They have telencephalic auditory areas specialized for processing natural sounds and considered as playing a critical role in the discrimination of behaviorally relevant vocal sounds. The zebra finch, a highly social songbird species, forms lifelong pair bonds. Only male zebra finches sing. However, both sexes produce the distance call when placed in visual isolation. This call is sexually dimorphic, is learned only in males and provides support for individual recognition in both sexes. Here, we assessed whether auditory processing of distance calls differs between paired males and females by recording spiking activity in a secondary auditory area, the caudolateral mesopallium (CLM), while presenting the distance calls of a variety of individuals, including the bird itself, the mate, familiar and unfamiliar males and females. In males, the CLM is potentially involved in auditory feedback processing important for vocal learning. Based on both the analyses of spike rates and temporal aspects of discharges, our results clearly indicate that call-evoked responses of CLM neurons are sexually dimorphic, being stronger, lasting longer, and conveying more information about calls in males than in females. In addition, how auditory responses vary among call types differ between sexes. In females, response strength differs between familiar male and female calls. In males, temporal features of responses reveal a sensitivity to the bird's own call. These findings provide evidence that sexual dimorphism occurs in higher-order processing areas within the auditory system. They suggest a sexual dimorphism in the function of the CLM, contributing to transmit information about the self-generated calls in males and to storage of information about the bird's auditory experience in females.

Auditory Responses to Vocal Sounds in the Songbird Nucleus Taeniae of the Amygdala and the Adjacent Arcopallium

“…This suggests the involvement of this auditory area in individual recognition [Menardy et al, 2012[Menardy et al, , 2014. Similarly, Giret et al [2015] showed that neurons in the caudolateral mesopallium exhibit different firing rate and spike patterns to different attributes of distance calls (including the degree of familiarity), and that such call-evoked responses were sexually dimorphic. Unlike these previous studies, we only demonstrated the existence of a neuronal population in the arcopallium sensitive to attributes of emitters.…”

“…Moreover, Woolley and Doupe [2008] reported that ZENK expression in female NCM reflects familiarity between the singer and the listener, whereas ZENK expression in CM reflects whether the song is directed or undirected. Responses of NCM and CM neurons to distance calls also reflect attributes of the calls including the emitters' sex, identity, and familiarity with the subjects [Gobes et al, 2009;Menardy et al, 2012Menardy et al, , 2014Giret et al, 2015].…”

Serotonin, estrus, and social context influence c-Fos immunoreactivity in the inferior colliculus.

“…Females may prefer particular types of male calls over others (e.g., Maney et al, 2003; Wilczynski & Lynch et al, 2011; Schubloom & Wooley, 2016; Brenowitz & Remage-Healey, 2016), and this preference behavior may track naturally varying reproductive status, or be influenced by the manipulation of ovarian hormones (Lynch et al, 2005; 2006; Ward et al, 2015). In parallel to this changing behavioral responsiveness, the auditory systems of females show preferential electrophysiological responses, or changes in immediate early gene expression, to male calls of particular structure, and these responses may also interact with variation in the hormonal milieu (Maney et al, 2006; Lynch & Wilczynski, 2008; Miranda & Wilczynski, 2009b; Svec & Wade, 2009; Chakraborty & Burmeister, 2015; Giret et al, 2015; Monbureau et al, 2015; Brenowitz & Remage-Healey, 2016). Peripheral or central changes in hormonal sensitivity may thus result in female auditory systems that are better matched to, more responsive to, or more discriminating of male signals (Forlano, et al, 2005; Sisneros, et al, 2004; Sisneros, 2009; Lynch & Wilczynski, 2008; Zeyl et al, 2013; Caras et al, 2015).…”

The effect of sex and menstrual phase on memory formation during a nap

“…Men and women differ across a range of laboratory tested cognitive domains including memory, visual and acoustic perception, navigation, and audition (Lewin et al, 2001;Canli et al, 2002;McDevitt E. A et al, 2014;Astur, R. S. et al, 1998;Giret et al, 2015;Murai et al, 1998;reviewed in Cahill, 2006). For example, memory performance that relies on the hippocampus, such as word and picture recall and recognition, story recall and name recognition is better in women than men (reviewed in Herlitz et al, 1999).…”