It takes a seasoned bird to be a good listener: communication between the sexes

Abstract

Birds commonly use sound for communication between the sexes. In many songbird species, only males sing and there are pronounced sex differences in the neural song control circuits. By contrast, the auditory circuitry is largely similar in males and females. Both sexes learn to recognize vocalizations heard as juveniles and this shapes auditory response selectivity. Mating vocalizations are restricted to the breeding season, when sex steroid levels are elevated. Auditory cells, from the ear to the cortex, are hormone sensitive. Estrogens are synthesized in the brain and can modulate the activity of auditory neurons. In species that breed seasonally, elevated levels of estradiol in females transiently enhance their auditory responses to conspecific vocalizations, resulting in sex differences in audition.

Figure 1. The neural circuits for auditory processing, song production, and sensorimotor learning in songbirds

The ascending pathway that processes auditory information including song is shown in blue. Auditory output from the inner ear is conveyed by the VIIIth nerve to the cochlear nuclei in the brain stem (not shown), and then to inferior colliculus (IC) in the midbrain [34]. IC projects to the nucleus ovoidalis (Ov) complex in the thalamus. Ov projects to the telencephalic field L complex (LI, L2, L3) (analogous to mammalian A1) and the caudomedial nidopallium (NCM, analogous to mammalian A2). The field L complex connects reciprocally to the caudomesopallium (CM, analogous to mammalian A2). NCM and CM are also reciprocally connected. There are sex differences in gene expression in NCM of Zebra Finches. Females show higher levels of calbindin expression, and males have more fibers in NCM that label for the estrogen synthesizing enzyme aromatase [50]. The nuclei in green represent the descending motor pathway for song production, which receives premotor information from the nuclei in purple. It originates in nucleus uvaeformis (Uva) in the thalamus and includes projections from HVC (proper name) to the robust nucleus of the acropallium (RA) in the telencephalon, and from RA to medullary nXIIts, which innervates the muscles of the sound-producing organ, the syrinx, and the brainstem respiratory pre-motor nuclei. An anterior forebrain pathway (AFP) important for song learning and vocal variability is shown in red. The AFP includes HVC, area × in the striatum, the dorso-lateral division of the medial thalamus (DLM, not shown), lateral magnocellular nucleus of the anterior nidopallium (LMAN), and RA; it is analogous to the mammalian basal ganglia-thalamocortical circuit [51]. The AFP is essential for song learning, for the motor production of song in juveniles [52], and for adult song variability [reviewed in 53]. The song control system receives auditory input at multiple levels. CM projects to ventral HVC, and to the area surrounding RA (not shown). CM also projects to the interfacial nucleus of the nidopallium (NIf), which appears to provide the major auditory input to the song control circuits (not shown) [reviewed in 54,55]. Neurons within HVC, RA, lMAN, area ×, and NIf respond to acoustic stimuli. Some neurons within each of these nuclei respond maximally, although not exclusively, to presentation of the bird’s own song (BOS), consistent with their primary role in sensorimotor integration.