Acute Aromatase Inhibition Impairs Neural and Behavioral Auditory Scene Analysis in Zebra Finches.

Auditory perception can be significantly disrupted by noise. To discriminate sounds from noise, auditory scene analysis (ASA) extracts the functionally relevant sounds from acoustic input. The zebra finch communicates in noisy environments. Neurons in their secondary auditory pallial cortex (caudomedial nidopallium, NCM) can encode song from background chorus, or scenes, and this capacity may aid behavioral ASA. Furthermore, song processing is modulated by the rapid synthesis of neuroestrogens when hearing conspecific song. To examine whether neuroestrogens support neural and behavioral ASA in both sexes, we retrodialyzed fadrozole (aromatase inhibitor, FAD) and recorded in vivo awake extracellular NCM responses to songs and scenes. We found that FAD affected neural encoding of songs by decreasing responsiveness and timing reliability in inhibitory (narrow-spiking), but not in excitatory (broad-spiking) neurons. Congruently, FAD decreased neural encoding of songs in scenes for both cell types, particularly in females. Behaviorally, we trained birds using operant conditioning and tested their ability to detect songs in scenes after administering FAD orally or injected bilaterally into NCM. Oral FAD increased response bias and decreased correct rejections in females, but not in males. FAD in NCM did not affect performance. Thus, FAD in the NCM impaired neuronal ASA but that did not lead to behavioral disruption suggesting the existence of resilience or compensatory responses. Moreover, impaired performance after systemic FAD suggests involvement of other aromatase-rich networks outside the auditory pathway in ASA. This work highlights how transient estrogen synthesis disruption can modulate higher-order processing in an animal model of vocal communication.

Social reinforcement guides operant behaviour and auditory learning in a songbird.

Motivation to seek social interactions is inherent to all social species. For instance, even with risk of disease transmission in a recent pandemic, humans sought out frequent in-person social interactions. In other social animals, socialization can be prioritized even over water or food consumption. Zebra finches, Taeniopygia guttata, are highly gregarious songbirds widely used in behavioural and physiological research. Songbirds, like humans, are vocal learners during development, which rely on intense auditory learning. Aside from supporting song learning, auditory learning further supports individual identification, mate choice and outcome associations in songbirds. To study auditory learning in a laboratory setting, studies often employ operant paradigms with food restriction and reinforcement and require complete social isolation, which can result in stress and other unintended physiological consequences for social species. Thus, in this work, we designed an operant behavioural method leveraging the sociality of zebra finches for goal-directed behaviours. Our approach relies on visual social reinforcement, without depriving the animals of food or social contact. Using this task, we found that visual social reinforcement was a strong motivational drive for operant behaviour. Motivation was sensitive to familiarity towards the stimulus animal and higher when engaging with a familiar versus a novel individual. We further show that this tool can be used to assess auditory discrimination learning using either songs or synthetic pure tones as stimuli. As birds gained experience in the task, they developed a strategy to maximize reward acquisition in spite of receiving more punishment, i.e. liberal response bias. Our operant paradigm provides an alternative to tasks using food reinforcement and could be applied to a variety of highly social species, such as rodents and nonhuman primates.

Black Jacobin hummingbirds vocalize above the known hearing range of birds.

Hummingbirds are a fascinating group of birds, but some aspects of their biology are poorly understood, such as their highly diverse vocal behaviors. We show here that the predominant vocalization of black jacobins (Florisuga fusca), a hummingbird prevalent in the mountains of the Brazilian Atlantic Forest, consists of a triplet of syllables with high fundamental frequency (mean F0 ∼11.8 kHz), rapid frequency oscillations and strong ultrasonic harmonics and no detectable elements below ∼10 kHz. These are the most common vocalizations of these birds, and their frequency range is above the known hearing range of any bird species recorded to date, including hearing specialists such as owls. These observations suggest that black jacobins either have an atypically high frequency hearing range, or alternatively their primary vocalization has a yet unknown function unrelated to vocal communication. Black jacobin vocalizations challenge current notions about vocal communication in birds.

Ultrasonic vocalizations in golden hamsters (Mesocricetus auratus) reveal modest sex differences and nonlinear signals of sexual motivation.

Vocal signaling is one of many behaviors that animals perform during social interactions. Vocalizations produced by both sexes before mating can communicate sex, identity and condition of the caller. Adult golden hamsters produce ultrasonic vocalizations (USV) after intersexual contact. To determine whether these vocalizations are sexually dimorphic, we analyzed the vocal repertoire for sex differences in: 1) calling rates, 2) composition (structural complexity, call types and nonlinear phenomena) and 3) acoustic structure. In addition, we examined it for individual variation in the calls. The vocal repertoire was mainly composed of 1-note simple calls and at least half of them presented some degree of deterministic chaos. The prevalence of this nonlinear phenomenon was confirmed by low values of harmonic-to-noise ratio for most calls. We found modest sexual differences between repertoires. Males were more likely than females to produce tonal and less chaotic calls, as well as call types with frequency jumps. Multivariate analysis of the acoustic features of 1-note simple calls revealed significant sex differences in the second axis represented mostly by entropy and bandwidth parameters. Male calls showed lower entropy and inter-quartile bandwidth than female calls. Because the variation of acoustic structure within individuals was higher than among individuals, USV could not be reliably assigned to the correct individual. Interestingly, however, this high variability, augmented by the prevalence of chaos and frequency jumps, could be the result of increased vocal effort. Hamsters motivated to produce high calling rates also produced longer calls of broader bandwidth. Thus, the sex differences found could be the result of different sex preferences but also of a sex difference in calling motivation or condition. We suggest that variable and complex USV may have been selected to increase responsiveness of a potential mate by communicating sexual arousal and preventing habituation to the caller.

Olfactory responses of neotropical short-tailed singing mice, Scotinomys teguina, to odors of the mid-ventral sebaceous gland: discrimination of conspecifics, gender, and female reproductive condition.

We examined the olfactory communication of the Neotropical short-tailed singing mouse, Scotinomys teguina, by investigating whether S. teguina responded to odors produced by the mid-ventral sebaceous gland of conspecifics. Females spent significantly more time investigating male odor than an odorless stimulus or a female odor. Males spent significantly more time investigating female odor than an odorless stimulus, but not that of a male odor. This latter result does not seem to be explained by differences in age or sexual experience of test subjects, but may be influenced by reproductive condition of the female odor donor. Male S. teguina spent significantly more time (1) investigating and (2) in total proximity to odors of estrous than non-estrous females. Males spent more time (1) investigating and (2) in total proximity to odors of males than non-estrous females. Finally, given the choice between odor of males vs proestrous females, males showed no preference. Thus, the mid-ventral gland in S. teguina seems to convey information about conspecifics, sex, and female reproductive condition. Male odor, compared with proestrous female odor, is equally interesting to males, suggesting that the gland also plays an important role in male-male communication. Sexual dimorphism in the size of the gland and in the amount of secretion produced by the gland may be related to either male-male competition or female choice.