Ventral midbrain stimulation induces perceptual learning and cortical plasticity in primates

John T Arsenault,Wim Vanduffel

doi:10.1038/s41467-019-11527-9

Abstract

Practice improves perception and enhances neural representations of trained visual stimuli, a phenomenon known as visual perceptual learning (VPL). While attention to task-relevant stimuli plays an important role in such learning, Pavlovian stimulus-reinforcer associations are sufficient to drive VPL, even subconsciously. It has been proposed that reinforcement facilitates perceptual learning through the activation of neuromodulatory centers, but this has not been directly confirmed in primates. Here, we paired task-irrelevant visual stimuli with microstimulation of a dopaminergic center, the ventral tegmental area (VTA), in macaques. Pairing VTA microstimulation with a task-irrelevant visual stimulus increased fMRI activity and improved classification of fMRI activity patterns selectively for the microstimulation-paired stimulus. Moreover, pairing VTA microstimulation with a task-irrelevant visual stimulus improved the subject’s capacity to discriminate that stimulus. This is the first causal demonstration of the role of neuromodulatory centers in VPL in primates.

Highlights

Practice improves perception and enhances neural representations of trained visual stimuli, a phenomenon known as visual perceptual learning (VPL)
We have shown that the association of ventral tegmental area (VTA)-EM and two entirely different task-irrelevant visual cues is sufficient to enhance the representation of these stimuli in primates
One of the defining features of VPL is its specificity with regard to the trained stimulus features, the position of the trained stimulus and even the trained eye24–28 - transfer has been observed in special circumstances[24,29]

Summary

Introduction

Practice improves perception and enhances neural representations of trained visual stimuli, a phenomenon known as visual perceptual learning (VPL). Task-irrelevant perceptual learning experiments offer an exception to this by demonstrating that Pavlovian stimulus-reward associations can generate VPL without attention oriented onto task-relevant stimuli[17,18] These studies indicate that neuromodulatory signals generated by rewards may be sufficient to drive stimulus selective learning. To test neuromodulatory theories of task-irrelevant learning in primates, we designed experiments to test whether the association of a task-irrelevant visual stimulus and electrical microstimulation of the VTA (VTA-EM)[19], a neuromodulatory center in the midbrain, is capable of generating the physiological and behavioral effects that typify VPL These experiments were designed to mimic task-relevant VPL paradigms whereby functional magnetic resonance imaging (fMRI) and behavior is measured before and after training. Our findings demonstrate a causal role for the VTA in visual cortical plasticity and VPL

Methods

Results

Conclusion