Training of goal-directed attention regulation enhances control over neural processing for individuals with brain injury

Abstract

Deficits in attention and executive control are some of the most common, debilitating and persistent consequences of brain injuries. Understanding neural mechanisms that support clinically significant improvements, when they do occur, may help advance treatment development. Intervening via rehabilitation provides an opportunity to probe such mechanisms. Our objective was to identify neural mechanisms that underlie improvements in attention and executive control with rehabilitation training. We tested the hypothesis that intensive training enhances modulatory control of neural processing of perceptual information in patients with acquired brain injuries. Patients (n=12) participated either in standardized training designed to target goal-directed attention regulation, or a comparison condition (brief education). Training resulted in significant improvements on behavioural measures of attention and executive control. Functional magnetic resonance imaging methods adapted for testing the effects of intervention for patients with varied injury pathology were used to index modulatory control of neural processing. Pattern classification was utilized to decode individual functional magnetic resonance imaging data acquired during a visual selective attention task. Results showed that modulation of neural processing in extrastriate cortex was significantly enhanced by attention regulation training. Neural changes in prefrontal cortex, a candidate mediator for attention regulation, appeared to depend on individual baseline state. These behavioural and neural effects did not occur with the comparison condition. These results suggest that enhanced modulatory control over visual processing and a rebalancing of prefrontal functioning may underlie improvements in attention and executive control.

Figures

Figure 1

Representative structural MRI images from participants with visible structural brain lesions.

Figure 2

Selection task performed during functional MRI data acquisition. Participants viewed a series of images composed of two categories (faces and scenes). In two selective attention conditions (select faces, select scenes) participants were instructed to selectively attend and hold in mind images from one category. The only difference across conditions was the task instructions, making particular image categories relevant or non-relevant, while the perceptual content did not differ across conditions. Solid and dashed lines are used only for purposes of illustrating task relevance, while only the greyscale images were used in the actual task.

Figure 3

Schematic of the determination of the clarity of information representation in brain activity patterns during the test block. In this example, inputs to the trained multi-layer perceptron are sampled patterns from scene stimulus trials (left) from either the Select Scenes condition (above) or Select Faces condition (below). The output node activations (right) reflect the classifier’s recognition of the pattern as representing a face or a scene stimulus. The magnitude of the difference between these output nodes indexes the certainty of classification for samples from a particular task condition. The effect of selective attention is indexed by the difference in certainty when an individual is instructed to select scenes versus select faces (i.e. the differential for when scenes are relevant versus non-relevant). This relevant to non-relevant differential is used as the primary measure for each brain region at each of the assessment time points.

Figure 4

Changes in attention and executive function composite scores for (A) goals training and (B) education. Bars represent change in z-scores (i.e. post-intervention minus pre-intervention z-score). The individual data are sorted based on magnitude of change, in order to illustrate descriptively the number of individuals with changes in the positive or negative direction with the goals training intervention, and participant identification numbers are matched to each subject’s scores pre- and post-education to facilitate direct comparison across intervention conditions.

Figure 5

Changes in index scores (relevant–non-relevant differential certainty scores) in (A) extrastriate cortex and (B) prefrontal cortex for goals training and education. Change scores were calculated by subtracting pre-intervention scores from post-intervention scores for goals training and for education. Data are presented sorted based on the magnitude of the change and individual subjects are matched across goals training and education.

Figure 6

Pre- and post-intervention scores for prefrontal cortex for (A) goals training and (B) education. Black bars represent pre-intervention scores, and white bars indicate post-intervention scores. Individual data are sorted by pre-intervention baseline score to illustrate the relationship between pre-intervention scores and pre- to post-intervention changes.