Prefrontal Cortex Activation While Walking Under Dual-Task Conditions in Stroke: A Multimodal Imaging Study

Abstract

Background Walking while performing another task (eg, talking) is challenging for many stroke survivors, yet its neural basis are not fully understood. Objective To investigate prefrontal cortex activation and its relationship to gait measures while walking under single-task (ST) and dual-task (DT) conditions (ie, walking while simultaneously performing a cognitive task) in stroke survivors. Methods We acquired near-infrared spectroscopy (NIRS) data from the prefrontal cortex during treadmill walking in ST and DT conditions in chronic stroke survivors and healthy controls. We also acquired functional magnetic resonance imaging (fMRI) and NIRS during simulated walking under these conditions. Results NIRS revealed increased oxygenated hemoglobin concentration in DT-walking compared with ST-walking for both groups. For simulated walking, NIRS showed a significant effect of group and group × task, being greater on both occasions, in stroke survivors. A greater increase in brain activation observed from ST to DT walking/ simulated walking was related to a greater change in motor performance in stroke survivors. fMRI revealed increased activity during DT relative to ST conditions in stroke patients in areas including the inferior temporal gyri, superior frontal gyri and cingulate gyri bilaterally, and the right precentral gyrus. The DT-related increase in fMRI activity correlated with DT-related change in behavior in stroke participants in the bilateral inferior temporal gyrus, left cingulate gyrus, and left frontal pole. Conclusion Our results provide novel evidence that enhanced brain activity changes relate to dual task motor decrements.

Keywords: cognitive motor interference; dual task; fMRI; gait control; near-infrared spectroscopy; prefrontal cortex; rehabilitation; stroke.

Figure 1

Experimental procedure: (A) Experiment 1. Participants completed 5 trials of each of the following tasks; walking alone (ST-walking), counting while standing (Counting), and walking while counting (DT-walking). Each trial consisted of a 30-second task period and alternated with rest periods in a pseudo-random order. (B) Experiment 2; one ABCD cycle. This cycle was repeated 6 times giving a total paradigm length of 12 minutes. The top row indicates when participants engaged in the counting task, the second row indicates when participants were moving their feet and the third row indicates the interaction between the 2 (ie, blocks when the 2 tasks were performed simultaneously). ST, single task; DT, dual task.

Figure 2

Near-infrared spectroscopy (NIRS) measurement: (A) Schematic representation of NIRS probe location. The red (transmitters) and blue (detectors) circles indicate positions of optodes. Numbers indicate the positions of channels defined as a midway between neighboring transmitter-detector pairs. The probe holder covered the area linking Fp1, F3, and F7 and the area linking Fp2, F4, and F8 according to the international 10-20 electroencephalography (EEG) system, which is correspondent to the left and right prefrontal cortex (PFC), respectively. (B and C) Representative examples of PFC activation in a stroke patient (B) and a healthy control (C) under single task (ST; dashed lines) and dual task (DT; solid lines) walking. Time course of the grand average across all blocks averaged over all measured probe positions (left and right PFC). The y-axis displays relative concentration changes of hemoglobin in millimoles per liter. The increase in [oxy-Hb] is indicated by the red line, the decrease in [deoxy-Hb] by the blue line. Vertical lines across the graphs indicate the 10-second time window used for further statistical analysis.

Figure 3

Group data (mean ± SD) of task-related changes in oxy-Hb (A and B) and deoxy-Hb (C and D) concentrations in the prefrontal cortex (PFC) during single-task (ST) and dual-task (DT) walking.

Figure 4

(A) Dual-task (DT)–related activation in stroke; thresholded images (Z > 2.3) of group for the positive interaction. Significant clusters defined according to extent (at corrected P < .01). (B) Group data (mean ± SD) of task-related changes in oxy-Hb concentrations in prefrontal cortex (PFC) during counting, ankle movement and DT as measured by near-infrared spectroscopy (NIRS) simultaneously with functional magnetic resonance imaging (fMRI).