Using a low-dimensional birdsong model to unveil neural coding in zebra finches

Fundamental unresolved problems of motor coding and sensorimotor integration include what information about behavior is represented at different levels of the motor pathway. An interdisciplinary collaboration integrating physical, acoustic, and biological approaches validated a dynamical systems model for birdsong production and proposed a novel frame for understanding neural coding in zebra finches.

HFSP Cross-Disciplinary Fellow Ana Amador and colleagues
authored on Thu, 27 February 2014

Songbirds are a well-established model system for studying the emergence of detailed motor skills, and in particular vocal learning, an ability shared by few other vertebrates. This animal system allows neural and peripheral recordings to be integrated with a precisely quantifiable behavior, the song. Although neural activity in the premotor forebrain nucleus, the HVC, has been related to song acoustics in auditory playback experiments, whether neural activity is related to song spectral structure during singing remains unresolved. To address this issue, we worked with a minimal physical model for birdsong production in which mathematical parameters can be linked to physiological properties, having as an output a synthetic song. Each syllable was coded in terms of parameters related to air sac pressure and tension of the syringeal labia, defining motor “gestures”. In order to validate this model, we assessed the responses of HVC neurons to song playback in sleeping birds. Under these conditions, HVC neurons exhibited selective responses to the bird's own song (BOS), and weaker responses to tones, noises, conspecific songs, or even slightly modified BOS. The output of the mathematical model (SYN) was able to elicit responses strikingly similar to those for BOS, with the same phasic-tonic features. These results demonstrate that a low dimensional model representing an approximation of peripheral mechanics is sufficient to capture behaviorally relevant features of song, providing important and valuable simplification that can help clarify neural coding.

Figure: Adult male zebra finch (left) uses his song to woo a female zebra finch (right). A low-dimensional dynamical systems model helps to unveil motor control in singing zebra finches.

Analyzing the HVC neurons' responses to playback of each bird’s own song, we observed that projection neurons were excited and interneurons were suppressed, with near-zero time lag, at the times of gesture extrema (defined as beginning, end or maxima of gestures). In this way, HVC neurons precisely encode the timing of extreme points of movement trajectories. We confirm these results with HVC recordings in singing birds. Our results suggest that movements are represented as trajectories at higher levels of motor systems. Given that HVC activity occurs with near synchrony to behavioral output, we propose a novel neural code in which the activity of HVC neurons represents the sequence of gestures in song making predictions on expected behavior.

Reference

Elemental gesture dynamics are encoded by song premotor cortical neuron. A. Amador, Y. Sanz Perl, G.B. Mindlin and D. Margoliash (2013). Nature 495: 59-64.

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