Meaning in the avian auditory cortex: neural representation of communication calls

Abstract

Understanding how the brain extracts the behavioral meaning carried by specific vocalization types that can be emitted by various vocalizers and in different conditions is a central question in auditory research. This semantic categorization is a fundamental process required for acoustic communication and presupposes discriminative and invariance properties of the auditory system for conspecific vocalizations. Songbirds have been used extensively to study vocal learning, but the communicative function of all their vocalizations and their neural representation has yet to be examined. In our research, we first generated a library containing almost the entire zebra finch vocal repertoire and organized communication calls along 9 different categories based on their behavioral meaning. We then investigated the neural representations of these semantic categories in the primary and secondary auditory areas of 6 anesthetized zebra finches. To analyze how single units encode these call categories, we described neural responses in terms of their discrimination, selectivity and invariance properties. Quantitative measures for these neural properties were obtained using an optimal decoder based both on spike counts and spike patterns. Information theoretic metrics show that almost half of the single units encode semantic information. Neurons achieve higher discrimination of these semantic categories by being more selective and more invariant. These results demonstrate that computations necessary for semantic categorization of meaningful vocalizations are already present in the auditory cortex and emphasize the value of a neuro-ethological approach to understand vocal communication.

How social learning adds up to a culture: from birdsong to human public opinion

“…Each of these call types is acoustically distinct and can be recognized as a distinct cluster in acoustic space. Acoustic variability within each of those call types is also meaningful, forming a rich, graded signal within each category, allowing birds to share a wide variety of behavioral states with their peers (Elie and Theunissen, 2015).…”

Audition and Hemispheric Specialization in Songbirds and New Evidence from Australian Magpies

“…While these areas (NCM and CM) were once just considered secondary auditory areas, they have now been recognized as important loci for conspecific song discrimination and individual song recognition and, as such, have behavioural significance [62][63][64][65][66][67]. Indeed, Woolley and colleagues [68] identified all nine functional areas in the forebrain and midbrain of the zebra finch (four in the midbrain alone), each of which was shown to play a specific role in extracting distinct complex sound features [68].…”

“…Strangely, 'repertoire size' in the literature, with a few exceptions [65], tends to mean the number of syllables in a song or total number of identifiably different songs a bird might sing, and is measured as such rather than as the sum total of vocalizations, not only song. To establish the true range of brain asymmetry or the lack thereof, it would seem important to consider the entire range of a bird's utterances (see Figure 2), since these are likely to represent different contexts and functions and may be under different neural control.…”

The Forebrain Song System Mediates Predictive Call Timing in Female and Male Zebra Finches

“…Although the forebrain song system is not required for producing short calls [12] or responding to them [10], birds appear to show plasticity in the timing of their calls. As in many social species that are vocal non-learners, the temporal patterns of calls produced by a group of zebra finches can be highly structured [13,14] which may reflect social bonds [15-17], reproductive state[18], and social hierarchy [19,20]. …”