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Report

Teaser, summary, work performed and final results

Periodic Reporting for period 1 - SavINGS (Locating Muscle Memory of Vocal Motor Skills)

Teaser

Summary

Complex motor skills, such as singing or playing an instrument, take much time and practice to learn while the brain and peripheral musculature adapt to the task. The acquired muscle coordination degrades when the skill is not used, but the previous level of control can be regained very rapidly with only little practice, a process termed savings. It is not well understood how savings come about, or where the information is stored that enables the quick retrieval of a previously learned motor skill.

Birdsong development provides an excellent experimental model to untangle the contributions of the central nervous system and periphery to vocal skill savings. By investigating plasticity in the songbird brain and periphery during the development, discontinuation, and rapid re-acquisition of vocal motor performance, we investigated where muscle memory is located and what mechanisms are involved in the retrieval of motor skills.

Our study demonstrates that the rapid re-acquisition of vocal skills in songbirds is accompanied by lasting modifications to the synaptic connectivity in the motor circuits that controls vocalizations. The observed synaptic changes could play an important role in the formation of vocal skill savings, enabling birds to rapidly re-acquire song performance at a later age.

This work helps identifying where motor memories are stored and what neural and peripheral mechanisms could be responsible for memorization and recall of motor skills. Furthermore, this work provides fundamental knowledge on possible mechanisms of how we learn new skills, how we maintain these skills as we grow older, and possibly how we can re-acquire skills that are lost through traumatic or neurodegenerative injuries.

Work performed

Motor learning involves the acquisition of a motor skill and its consolidation into memory, two distinct processes with separate neural substrates. Although the motor cortex has been implicated in the early consolidation of motor skills, it is unclear what constitutes the long-term memorization of these skills and how the peripheral musculature can quickly re-acquire motor performance after long periods of non-use.

To investigate this issue, we used birdsong acquisition as a model system, as songbirds have evolved a well-described specialized neural motor circuitry and vocal organ, both dedicated exclusively to song.

First, we determined the contribution of synaptic plasticity in the brain circuitry controlling singing behaviour to skill savings. One of the song control areas in the songbird forebrain, nucleus HVC, is located at a central position in the motor circuitry that drives the the songbird vocal organ, the syrinx. We analyzed the the density of neuronal dendritic spines, the loci where most of the synaptic connections are formed, in HVC at different stages during the development, loss, and re-development of song. We found that the number of spines in HVC strongly reduces when a bird develops song for the first time. Moreover, this reduction is maintained when birds stop singing, suggesting that a lasting memory has formed that could enable birds to quickly re-acquire song performance (Vellema et al., 2018; BioRxiv doi: https://doi.org/10.1101/440388).

Secondly, we investigated the contribution of vocal muscles during vocal skill development. The songbird vocal organ, the syrinx, is a well-described bipartite structure specifically adapted for producing the high variety of sounds that is unique to birdsong. Eight pairs of muscles envelop the two sound sources that can be operated independently to increase vocal performance. Because we previously found that the speed of vocal muscles increases significantly during song development (Mead et al., eLife 2017; 6: e29425), and influences motor behaviors on a millisecond scale (Srivastava, K., 2017; Proc. Natl. Acad. Sci. U.S.A. 114: 1171-1176), we investigated if muscle speeds were maintained between periods of song development. We quantified muscle kinetics during the development, loss, and redevelopment of song, and found no direct evidence that muscles are involved in storing motor skills.

Together these results suggest that during development motor skills are stored in the brain circuits that control the behaviour in question, and quickly drive the peripheral musculature towards previously acquired motor performance.

Final results

Skill savings are evident in day-to-day life, but the neurophysiological mechanisms that are involved in the rapid return of previously learned skills are not well understood. Motor savings do not only rely on the central nervous system, but also on the biomechanical properties of the periphery, two levels of control that are seldom studied together.

Here we established the recurring acquisition of song performance as a new model system to study motor skill savings. Because both the central and peripheral mechanisms behind motor savings can be studied directly within the same behavioural model system, this model system opens up a wealth of new experimental possibilities for Behavioural Neuroscience.

Using this model system we generated valuable new insights into the fundamental mechanisms behind motor skill savings. This new knowledge has wide implications for the field of Neuroscience in general and can be exploited for further research activities on motor skill learning. The fundamental insights from this project may ultimately contribute to our understanding of how constraints on motor skill learning may be overcome in disease and injury, and lead to new implications for therapies of speech impairments and other motor disorders.