Hypothalamic Neurons Preferentially Respond to Female Nest Coo Stimulation: Demonstration of Direct Acoustic Stimulation of Luteinizing Hormone Release

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Abstract
Avian vocalizations are generally understood to play a pivotal role in reproductive functions. The role of the hypothalamus in gonadotropin release in higher vertebrates including birds is well established. To date, however, a direct linkage between the neuronal processing of vocal input and the contingent luteinizing hormone (LH) response has not been demonstrated. In this study, using female ring doves, we recorded neuronal activity from hypothalamic nuclei that, as we have shown previously, receive acoustic inputs from the auditory thalamic relay. Concurrently with recording single-unit responses to stimulation with species-specific coo vocalizations, we sampled LH levels in blood from the pituitary veins. LH concentration in the plasma was significantly elevated in birds hearing species-typical coos but not in birds exposed to experimentally altered coos or white noise or in birds that received no vocal stimulation. We found two types of neurons in the preoptic and anterior hypothalamus that selectively responded to the female nest coo: excitatory units and inhibitory units. Among the excitatory neurons are units characterized by two bursts separated by a period of slow spiking or complete silence, in a pattern approximately corresponding temporally to the two-note coo. We designate them as female-nest-coo-specific units. Most neurons in the posterior hypothalamus were nonselective in their response. Female nest coo and male nest coo stimulation evoked an equal magnitude of discharge changes from responsive units in the preoptic-anterior hypothalamic area. We found, however, that the LH increment was three times greater for birds hearing female nest coos than for birds hearing male nest coos. These observations suggest that feature-detecting neurons such as the female-nest-coo-specific units are involved in gonadotropin-releasing hormone output. The present findings are consistent with the well established behavioral evidence that female nest coos mediate ovarian growth.