Advantages of comparative studies in songbirds to understand the neural basis of sensorimotor integration

Abstract

Sensorimotor integration is the process through which the nervous system creates a link between motor commands and associated sensory feedback. This process allows for the acquisition and refinement of many behaviors, including learned communication behaviors such as speech and birdsong. Consequently, it is important to understand fundamental mechanisms of sensorimotor integration, and comparative analyses of this process can provide vital insight. Songbirds offer a powerful comparative model system to study how the nervous system links motor and sensory information for learning and control. This is because the acquisition, maintenance, and control of birdsong critically depend on sensory feedback. Furthermore, there is an incredible diversity of song organizations across songbird species, ranging from songs with simple, stereotyped sequences to songs with complex sequencing of vocal gestures, as well as a wide diversity of song repertoire sizes. Despite this diversity, the neural circuitry for song learning, control, and maintenance remains highly similar across species. Here, we highlight the utility of songbirds for the analysis of sensorimotor integration and the insights about mechanisms of sensorimotor integration gained by comparing different songbird species. Key conclusions from this comparative analysis are that variation in song sequence complexity seems to covary with the strength of feedback signals in sensorimotor circuits and that sensorimotor circuits contain distinct representations of elements in the vocal repertoire, possibly enabling evolutionary variation in repertoire sizes. We conclude our review by highlighting important areas of research that could benefit from increased comparative focus, with particular emphasis on the integration of new technologies.

Behavioural responses to video and live presentations of females reveal a dissociation between performance and motivational aspects of birdsong

“…From a mechanistic perspective, these data also suggest that videos of females engage the neural circuits for song performance to a comparable extent as live presentations of females. Neural activity in the anterior forebrain pathway (AFP) regulates context-dependent changes in the variability of fundamental frequency (reviewed in Brainard and Doupe, 2013; Murphy et al, 2017; Sakata and Vehrencamp, 2012; Woolley and Kao, 2015), whereas neural activity in the vocal motor pathway (VMP) has been proposed regulate context-dependent changes to temporal features of songs such as song tempo or the number of introductory notes before song (Aronov and Fee, 2012; Hampton et al, 2009; Matheson et al, 2016; Murphy et al, 2017; Rajan and Doupe, 2013; Stepanek and Doupe, 2010). Our data suggest that videos of females modulate neural activity in these circuits in the same way and to the same extent as live females.…”

Caudal mesopallial neurons in female songbirds bridge sensory and motor brain regions

“…Bidirectional connectivity between CM and NC has been described previously (Vates et al, ), and those interconnected sites are often collectively referred to as the “auditory lobule” of the songbird brain (Cheng & Clayton, ; London & Clayton, ). The auditory lobule is implicated in song learning in juvenile males and is thought to facilitate the development of song preferences in juvenile female songbirds (Amin, Doupe, & Theunissen, ; Gobes & Bolhuis, ; London & Clayton, ; Murphy, James, Sakata, & Prather, ). Similar to CM, the activity of the neurons within NC is selective for natural vocalizations, and that selectivity may help females to assign identity to the vocalizations of specific individuals (Menardy et al, ).…”

The function and failure of sensory predictions

“…In summary, suppression of auditory cortical activity in response to self‐produced versus externally generated sounds provides evidence for the presence of a predictive mechanism originating in motor/speech production areas, potentially mediated by CD signals. Our review focuses on studies conducted in humans and monkeys, but it is important to note that CD mechanisms producing inhibition of auditory areas during self‐induced sound, such as singing, are present across species, for example, in songbirds or crickets . Moreover, CD signals are not only critical for the discrimination of self‐produced versus externally generated sounds, but they also enable higher level functions such as learning of acoustic behavior, speech, and music across species by suppressing auditory responses to movement‐related stimulation .…”