In Humans, fMRI Reveals That Striosome-like and Matrix-like Striatal Voxels are Engaged in Different Phases of Movement

Introduction

The striatum is organized into two neurochemically and anatomically distinct compartments, the striosome and matrix, that play specialized roles in motor and cognitive functions. While extensive animal research has elucidated compartment-specific contributions to reward, learning and motor control, direct evidence for compartment specialization in humans is lacking.

Methods

We defined human striatal voxels as striosome-like or matrix-like based on biases in structural (diffusion) connectivity. Then we investigated functional activation patterns in those compartment-like voxels using task-based functional MRI (tfMRI) during pre-movement cue and five motor conditions (left/right hand, left/right foot, and tongue movements).

Results

Functional activation was strikingly segregated: striosome-like voxels were preferentially engaged during the cue phase, while matrix-like voxels dominated activation during motor execution, especially for tongue and foot movement. Motor tasks elicited robust bilateral activation, with contralateral activation dominating during limb movements. Activation was more lateralized in matrix-like than in striosome-like voxels. Both striosome-like and matrix-like voxels exhibited strong activation at the onset of task execution (e.g., within the first few seconds post-cue). However, activation in matrix-like voxels declined modestly over the course of the movement phase, while striosomal activation dropped sharply at task termination, suggesting a role in behavioral transitions. These findings are consistent with the role of the striosome in anticipatory evaluation and dopaminergic modulation, and matrix specialization for executing automatized routines.

Conclusions

This study provides the first task-based fMRI evidence of temporally and functionally distinct striatal compartment dynamics in humans, offering novel insights into striatal microcircuitry in motivated behavior and the planning and execution of movements.

Key Points

• Striatal medium spiny neurons develop in two interdigitated tissue compartments, the striosome and matrix, that are embryologically, pharmacologically, and anatomically distinct. Inter-compartmental differences in function have been identified in animals, but never in humans.

• We found that in humans, the compartments differed in functional activation during movement tasks: during the task cue, activation was greater in striosome-like voxels, while matrix-like activation was greater during each of five distinct types of movement.

• Both compartments were active at the beginning of movement, but at the termination of movement striosome-like activation fell to below baseline, suggesting a role for the striosome in behavioral transitions.