Combined effect of prefrontal transcranial direct current stimulation and a working memory task on heart rate variability

Abstract

Prefrontal cortex activity has been associated with changes to heart rate variability (HRV) via mediation of the cortico-subcortical pathways that regulate the parasympathetic and sympathetic branches of the autonomic nervous system. Changes in HRV due to altered prefrontal cortex functioning can be predicted using the neurovisceral integration model, which suggests that prefrontal hyperactivity increases parasympathetic tone and decreases contributions from the sympathetic nervous system. Working memory (WM) tasks and transcranial direct current stimulation (tDCS) have been used independently to modulate brain activity demonstrating changes to HRV in agreement with the model. We investigated the combined effects of prefrontal tDCS and a WM task on HRV. Bifrontal tDCS was administered for 15 minutes at 2mA to 20 participants in a sham controlled, single-blind study using parallel groups. A WM task was completed by participants at three time points; pre-, during-, and post-tDCS, with resting state data collected at similar times. Frequency-domain HRV was computed for high frequency (HF; 0.15-0.4Hz) and low frequency (LF; 0.04-0.15Hz) power reflecting parasympathetic and sympathetic branch activity, respectively. Response time on the WM task, but not accuracy, improved from baseline to during-tDCS and post-tDCS with sham, but not active, stimulation. HF-HRV was significantly increased in the active tDCS group compared to sham, lasting beyond cessation of stimulation. Additionally, HF-HRV showed a task-related reduction in power during performance on the WM task. Changes in LF-HRV were moderately inversely correlated (r > 0.4) with changes in WM accuracy during and following tDCS compared to baseline levels. Stimulation of the prefrontal cortex resulted in changes to the parasympathetic branch of the nervous system in agreement with a linearly additive interpretation of effects. Sympathetic activity was not directly altered by tDCS, but was correlated with changes in WM performance. This suggests that the parasympathetic and sympathetic branches respond differentially due to similar, but distinct neural pathways. Given the ease of HRV data collection, studies of prefrontal tDCS would benefit from collection of this data as it provides unique insight into tDCS effects resulting from propagation through brain networks.

Fig 1. Neurovisceral integration model.

(A) Simplified depiction of the neurovisceral integration model described by Thayer and Sternberg [1]. (B) Brain regions relevant to the neurovisceral integration model. PC, prefrontal cortex; CC, cingulate cortex; Hyp, hypothalamus; Ins, insula; Amy, amygdala; BS, brainstem.

Fig 2. Study design using parallel groups.

HRV data was collected at five epochs, each lasting five minutes. ECG data were recorded at periods of rest occurring at baseline, as well as during-tDCS and post-tDCS, in addition to task-related activity during-tDCS and post-tDCS. Shaded block indicates period during which tDCS was administered.

Fig 3. Working memory scores.

(A) Participants receiving sham-tDCS improved in response time from baseline to during-tDCS and post-tDCS time points. (B) Working memory accuracy scores calculated as percentage of correct responses. Error bars represent standard deviations. * p < .05.

Fig 4. Results of baseline-corrected electrocardiogram HRV analyses using estimated marginal means from mixed effects model analysis.

(A) High frequency (HF) power. (B) Low frequency (LF) power. Error bars represent standard deviations. * p < .05.

Fig 5. Correlation between the change in working memory accuracy and change in LF power.

(A) change from baseline to during-tDCS task period; and (B) change from baseline to post-tDCS task period.