Two neural streams, one voice: Pathways for theme and variation in the songbird brain

Highlights

• Birdsong is learned in a manner similar to human speech.

• Two premotor pathways generate the theme and variation of song, but their relative influence shifts during learning.

• In adult birds, auditory feedback and social stimuli influence the gain of the dual premotor pathways.

• The neural composition of birdsong involves axial swaths of interconnected neurons.

Abstract

Birdsong offers a unique model system to understand how a developing brain – once given a set of purely acoustic targets – teaches itself the vocal-tract gestures necessary to imitate those sounds. Like human infants, to juvenile male zebra finches (Taeniopygia guttata) falls the burden of initiating the vocal-motor learning of adult sounds. In both species, adult caregivers provide only a set of sounds to be imitated, with little or no information about the vocal-tract gestures used to produce the sounds. Here, we focus on the central control of birdsong and review the recent discovery that zebra finch song is under dual premotor control. Distinct forebrain pathways for structured (theme) and unstructured (variation) singing not only raise new questions about mechanisms of sensory-motor integration, but also provide a fascinating new research opportunity. A cortical locus for a motor memory of the learned song is now firmly established, meaning that anatomical, physiological, and computational approaches are poised to reveal the neural mechanisms used by the brain to compose the songs of birds.

Introduction

Among various forms of developmentally-regulated learning, birdsong most resembles human speech learning. Similar to human infants, juvenile male zebra finches learn to imitate a paternal vocal pattern in a two-phase process that proceeds with little or no requirement for external reinforcement. The initial ‘sensory’ phase involves the formation of an auditory memory of the paternal vocal pattern. Notably, the memory contains only the product of the paternal vocal behavior – the acoustic structure and sequence of vocal sounds. As with human speech there is minimal transmission of information about how to produce the sounds.

In zebra finches, the subsequent ‘sensory-motor’ stage of learning overlaps the initial sensory stage. Sensory-motor learning begins with highly unstructured singing (termed ‘subsong’) that resembles the vocal babbling of human infants (see Fig. 1A). As the name implies, sensory-motor learning requires sensory feedback of the juvenile bird’s own vocalizations for song to be learned. Of critical importance is auditory feedback, which references the auditory memory of paternal song acquired during sensory learning (Price, 1979, Funabiki and Konishi, 2003). Interestingly, the variable structure of subsong appears to be a purposeful exploration of the dynamic range of the vocal organ (Ölveczky et al., 2005, Aronov et al., 2008, Thompson et al., 2011), and perhaps provides a period of associative learning where relationships between different vocal gestures and the sounds those gestures produce are discovered. Subsong is followed by plastic song, characterized by the emergence of a spectrally-pluripotent class of syllables (protosyllables) that progressively differentiate in a piecemeal fashion into facsimiles of the syllables and syllable sequences present in the paternal song pattern (Tchernichovski et al., 2001, Miller et al., 2010, Ravbar et al., 2012, Lipkind et al., 2013 and Fig. 1B). As male zebra finches reach adulthood (90–120 days post-hatch) the song pattern consolidates into a motor memory that is subsequently referenced and produced throughout adult life as a behavioral marker of a bird’s paternal lineage.