Life-Stage Dependent Plasticity in the Auditory System of a Songbird Is Signal and Emitter-Specific

Abstract

Social animals flexibly use a variety of vocalizations to communicate in complex and dynamic environments. However, it remains unknown whether the auditory perception of different vocalizations changes according to the ecological context. By using miniature wireless devices to synchronously record vocal interactions and local neural activity in freely-behaving zebra finches in combination with playback experiments, we investigate whether the auditory processing of vocalizations changes across life-history stages. We show that during breeding, females (but not males) increase their estrogen levels and reply faster to their mates when interacting vocally. These changes are associated with an increase in the amplitude of the female’s neural auditory responses. Furthermore, the changes in auditory response are not general, but specific to a subset of functionally distinct vocalizations and dependent on the emitter’s identity. These results provide novel insights into auditory plasticity of communication systems, showing that the perception of specific signals can shift according to ecologically-determined physiological states.

Cortical representation of group social communication in bats

“…These interactions are commonly mediated by vocal communication signals that convey social information, such as participant identity, context, and social preferences (1)(2)(3). Substantial progress has been made toward investigating the neural representation of sensory, motor, and social aspects of vocalizations separately (4)(5)(6)(7)(8), but rarely have all aspects been examined together (9) or in a group setting where behavioral and neural activity were recorded from more than two animals simultaneously. As a result, our ability to connect behavior and neural activity has been limited to individuals or pairs, rather than groups; consequently, it has been difficult to explore the specific social and neural relationships that exist within a group (10).…”

Reciprocal processes of sensory perception and social bonding: an integrated social‐sensory framework of social behavior

“…Furthermore, temporary inactivation of the female NCM decreases song and mate choice discrimination and modulates patterns of affiliation between partners 186 . Finally, in both male and female NCM, patterns of NCM neuronal activity are modulated in behaviorally relevant ways based on call type, the identity of the sender, and the breeding context 184 . Such plasticity within the NCM demonstrates how interactions between social and sensory experiences alter brain anatomy and function.…”

“…Social experience and signal salience are hypothesized to be encoded within the auditory region the caudomedial nidopallium (NCM) 183 . In females, the neuronal spiking activity in NCM is higher in response to hearing a familiar call 183,184 and V1aR density is higher in NCM after pairing 185 . Furthermore, temporary inactivation of the female NCM decreases song and mate choice discrimination and modulates patterns of affiliation between partners 186 .…”

Mechanisms, development, and comparative perspectives on experience‐dependent plasticity in social behavior

“…Mating is known to affect hormonal responses in birds, and hormonal responses have well‐documented effects on sensory plasticity (Adreani et al, 2020; Madison et al, 2018; Remage‐Healey et al, 2003; Tobari & Tsutsui, 2019). For example, neural and behavioral responses to vocal signals have been shown to differ in breeding versus nonbreeding individuals (Adreani et al, 2020; Maney & Pinaud, 2011).…”

“…Mating is known to affect hormonal responses in birds, and hormonal responses have well‐documented effects on sensory plasticity (Adreani et al, 2020; Madison et al, 2018; Remage‐Healey et al, 2003; Tobari & Tsutsui, 2019). For example, neural and behavioral responses to vocal signals have been shown to differ in breeding versus nonbreeding individuals (Adreani et al, 2020; Maney & Pinaud, 2011). Moreover, local application of estrogen alters the activity of song‐responsive neurons in the secondary auditory cortex (Caras & Remage‐Healey, 2016; Remage‐Healey et al, 2010; Remage‐Healey, 2020), suggesting that physiological changes caused by breeding influence the perceptual processing of auditory signals.…”