Neural mechanisms of auditory species recognition in birds

Abstract

Auditory communication in humans and other animals frequently takes place in noisy environments with many co-occurring signallers. Receivers are thus challenged to rapidly recognize salient auditory signals and filter out irrelevant sounds. Most bird species produce a variety of complex vocalizations that function to communicate with other members of their own species and behavioural evidence broadly supports preferences for conspecific over heterospecific sounds (auditory species recognition). However, it remains unclear whether such auditory signals are categorically recognized by the sensory and central nervous system. Here, we review 53 published studies that compare avian neural responses between conspecific versus heterospecific vocalizations. Irrespective of the techniques used to characterize neural activity, distinct nuclei of the auditory forebrain are consistently shown to be repeatedly conspecific selective across taxa, even in response to unfamiliar individuals with distinct acoustic properties. Yet, species-specific neural discrimination is not a stereotyped auditory response, but is modulated according to its salience depending, for example, on ontogenetic exposure to conspecific versus heterospecific stimuli. Neuromodulators, in particular norepinephrine, may mediate species recognition by regulating the accuracy of neuronal coding for salient conspecific stimuli. Our review lends strong support for neural structures that categorically recognize conspecific signals despite the highly variable physical properties of the stimulus. The available data are in support of a 'perceptual filter'-based mechanism to determine the saliency of the signal, in that species identity and social experience combine to influence the neural processing of species-specific auditory stimuli. Finally, we present hypotheses and their testable predictions, to propose next steps in species-recognition research into the emerging model of the neural conceptual construct in avian auditory recognition.

Keywords: auditory forebrain; imprinting; object recognition; ornithology; sexual selection; species recognition; vocal learning.