title: Single Neurons in the Avian Auditory Cortex Encode Individual Identity and Propagation Distance in Naturally Degraded Communication Calls.
abstract: One of the most complex tasks performed by sensory systems is "scene analysis": the interpretation of complex signals as behaviorally relevant objects. The study of this problem, universal to species and sensory modalities, is particularly challenging in audition, where sounds from various sources and localizations, degraded by propagation through the environment, sum to form a single acoustical signal. Here we investigated in a songbird model, the zebra finch, the neural substrate for ranging and identifying a single source. We relied on ecologically and behaviorally relevant stimuli, contact calls, to investigate the neural discrimination of individual vocal signature as well as sound source distance when calls have been degraded through propagation in a natural environment. Performing electrophysiological recordings in anesthetized birds, we found neurons in the auditory forebrain that discriminate individual vocal signatures despite long-range degradation, as well as neurons discriminating propagation distance, with varying degrees of multiplexing between both information types. Moreover, the neural discrimination performance of individual identity was not affected by propagation-induced degradation beyond what was induced by the decreased intensity. For the first time, neurons with distance-invariant identity discrimination properties as well as distance-discriminant neurons are revealed in the avian auditory cortex. Because these neurons were recorded in animals that had prior experience neither with the vocalizers of the stimuli nor with long-range propagation of calls, we suggest that this neural population is part of a general-purpose system for vocalizer discrimination and ranging.SIGNIFICANCE STATEMENTUnderstanding how the brain makes sense of the multitude of stimuli that it continually receives in natural conditions is a challenge for scientists. Here we provide a new understanding of how the auditory system extracts behaviorally relevant information, the vocalizer identity and its distance to the listener, from acoustic signals that have been degraded by long-range propagation in natural conditions. We show, for the first time, that single neurons, in the auditory cortex of zebra finches, are capable of discriminating the individual identity and sound source distance in conspecific communication calls. The discrimination of identity in propagated calls relies on a neural coding that is robust to intensity changes, signals' quality, and decreases in the signal-to-noise ratio.
authors.affiliation: Equipe de Neuro-Ethologie Sensorielle-Neuro-PSI CNRS UMR9197, Université de Lyon/Saint-Etienne, 42023 Saint-Etienne, France, and solveig.mouterde@uclouvain.be.|Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720, and.
authors.forename: Solveig C
authors.identifier: 0000-0002-4170-0252
authors.initials: SC
authors.lastname: Mouterde
authors.affiliation: Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720, and.
authors.forename: Julie E
authors.identifier: 0000-0002-7993-0264
authors.initials: JE
authors.lastname: Elie
authors.affiliation: Equipe de Neuro-Ethologie Sensorielle-Neuro-PSI CNRS UMR9197, Université de Lyon/Saint-Etienne, 42023 Saint-Etienne, France, and.
authors.forename: Nicolas
authors.identifier: 0000-0003-0219-6601
authors.initials: N
authors.lastname: Mathevon
authors.affiliation: Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720, and.|Department of Psychology, University of California, Berkeley, California 94720.
authors.forename: Frédéric E
authors.identifier: 0000-0001-8980-0650
authors.initials: FE
authors.lastname: Theunissen
mesh_terms: D000161:Acoustic Stimulation / Q000379:methods; D000200:Action Potentials / Q000502:physiology*; D000819:Animal Communication; D000818:Animals; D001303:Auditory Cortex / Q000502:physiology*; D005260:Female; D046369:Finches / Q000502:physiology*; D008297:Male; D011984:Sensory Receptor Cells / Q000502:physiology*; D012933:Social Identification; D012951:Socialization
keywords: auditory scene analysis; electrophysiology; ranging; songbird; sound propagation; vocal communication