Abstract

Direct manipulation of brain activity can be used to investigate causal brain-behavior relationships. Current noninvasive neural stimulation techniques are too coarse to manipulate behaviors that correlate with fine-grained spatial patterns recorded by fMRI. However, these activity patterns can be manipulated by having people learn to self-regulate their own recorded neural activity. This technique, known as fMRI neurofeedback, faces challenges as many participants are unable to self-regulate. The causes of this non-responder effect are not well understood due to the cost and complexity of such investigation in the MRI scanner. Here, we investigated the temporal dynamics of the hemodynamic response measured by fMRI as a potential cause of the non-responder effect. Learning to self-regulate the hemodynamic response involves a difficult temporal credit-assignment problem because this signal is both delayed and blurred over time. Two factors critical to this problem are the prescribed self-regulation strategy (cognitive or automatic) and feedback timing (continuous or intermittent). Here, we sought to evaluate how these factors interact with the temporal dynamics of fMRI without using the MRI scanner. We first examined the role of cognitive strategies by having participants learn to regulate a simulated neurofeedback signal using a unidimensional strategy: pressing one of two buttons to rotate a visual grating that stimulates a model of visual cortex. Under these conditions, continuous feedback led to faster regulation compared to intermittent feedback. Yet, since many neurofeedback studies prescribe implicit self-regulation strategies, we created a computational model of automatic reward-based learning to examine whether this result held true for automatic processing. When feedback was delayed and blurred based on the hemodynamics of fMRI, this model learned more reliably from intermittent feedback compared to continuous feedback. These results suggest that different self-regulation mechanisms prefer different feedback timings, and that these factors can be effectively explored and optimized via simulation prior to deployment in the MRI scanner.

Highlights

  • Neuroimaging studies often find correlations between behaviors and recorded neural activation

  • While millimeter-scale patterns cannot yet be targeted with noninvasive brain stimulation, some people can learn to self-stimulate these activity patterns if they receive real-time feedback of their own recorded brain activity through a procedure known as functional magnetic resonance imaging (fMRI) neurofeedback

  • Because experiments in the MRI scanner are costly and time-consuming, we created a simulated neurofeedback environment to compare continuous versus intermittent feedback timing and cognitive versus automatic self-regulation strategies

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Summary

Introduction

Neuroimaging studies often find correlations between behaviors and recorded neural activation. Safe and noninvasive neural stimulation techniques such as transcranial magnetic stimulation (TMS) and transcranial direct-current stimulation (tDCS) can only affect neural structures on the scale of centimeters [1, 2]. These techniques are too coarse to manipulate behaviors that correlate with the millimeter-scale patterns of neural activation recorded by functional magnetic resonance imaging (fMRI). Using multi-voxel pattern analysis (MVPA [3]), we can identify neural features such as orientation tuning [4, 5] and complex motor programs [6, 7] which are inaccessible to other human neuroimaging analysis methods

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