What Is the Role of Thalamostriatal Circuits in Learning Vocal Sequences?

Lei Xiao,Todd F Roberts

doi:10.3389/fncir.2021.724858

Abstract

Basal ganglia (BG) circuits integrate sensory and motor-related information from the cortex, thalamus, and midbrain to guide learning and production of motor sequences. Birdsong, like speech, is comprised of precisely sequenced vocal elements. Learning song sequences during development relies on Area X, a vocalization related region in the medial striatum of the songbird BG. Area X receives inputs from cortical-like pallial song circuits and midbrain dopaminergic circuits and sends projections to the thalamus. It has recently been shown that thalamic circuits also send substantial projections back to Area X. Here, we outline a gated-reinforcement learning model for how Area X may use signals conveyed by thalamostriatal inputs to direct song learning. Integrating conceptual advances from recent mammalian and songbird literature, we hypothesize that thalamostriatal pathways convey signals linked to song syllable onsets and offsets and influence striatal circuit plasticity via regulation of cholinergic interneurons (ChIs). We suggest that syllable sequence associated vocal-motor information from the thalamus drive precisely timed pauses in ChIs activity in Area X. When integrated with concurrent corticostriatal and dopaminergic input, this circuit helps regulate plasticity on medium spiny neurons (MSNs) and the learning of syllable sequences. We discuss new approaches that can be applied to test core ideas of this model and how associated insights may provide a framework for understanding the function of BG circuits in learning motor sequences.

Highlights

The ability to adeptly sequence motor actions is central to animal survival, coordinated movement, and communication
Ablation of thalamic inputs to the dorsolateral striatum (DLS) prevents naïve rats from learning a new motor sequence and revert the performance of motor sequences in expert rats to levels similar to those observed in the early phases of learning (Hidalgo-Balbuena et al, 2019; Wolff et al, 2019). These results argue that thalamostriatal projections may be relevant in driving the dorsal striatum and necessary to perform a sequence of learned motor actions
We propose a gated-reinforcement learning model, which takes thalamostriatal input as well as cholinergic interneurons (ChIs) pauses into consideration to help resolve credit assignment for song syllables in vocal learning (Figures 1D,2D)

Summary

INTRODUCTION

The ability to adeptly sequence motor actions is central to animal survival, coordinated movement, and communication. We propose that Area X receives three distinct streams of information about a song: a detailed timestamp for each moment in the song from HVC, a signal about the variability of spectral content at each moment from LMAN, and information about syllable onsets and offsets that permits syllable-level chunking of behavior from DLM Together, these three inputs may provide essential substrates to support the learning of spectral features in syllables as well as syllable sequences. We propose a gated-reinforcement learning model, which takes thalamostriatal input as well as ChI pauses into consideration to help resolve credit assignment for song syllables in vocal learning (Figures 1D,2D) In this model, two independent components constitute the third factor used to modulate Hebbian plasticity in Area X: a reward prediction error signal, similar to that implemented in the above model, and a top-down feedback signal, often referred to as an attentional signal (Roelfsema and Van Ooyen, 2005; Rombouts et al, 2015; Kusmierz et al, 2017). We cannot exclude other possible mechanisms that can contribute to pauses in ChIs, such as midbrain dopamine input and/or GABAergic input from the midbrain or some other source (Lim et al, 2014; Zhang and Cragg, 2017; Ahmed et al, 2019)

DISCUSSION

DATA AVAILABILITY STATEMENT