Disruption and rescue of interareal theta phase coupling and adaptive behavior

Abstract

Rescuing executive functions in people with neurological and neuropsychiatric disorders has been a major goal of psychology and neuroscience for decades. Innovative computer-training regimes for executive functions have made tremendous inroads, yet the positive effects of training have not always translated into improved cognitive functioning and often take many days to emerge. In the present study, we asked whether it was possible to immediately change components of executive function by directly manipulating neural activity using a stimulation technology called high-definition transcranial alternating current stimulation (HDtACS). Twenty minutes of inphase stimulation over medial frontal cortex (MFC) and right lateral prefrontal cortex (lPFC) synchronized theta (∼6 Hz) rhythms between these regions in a frequency and spatially specific manner and rapidly improved adaptive behavior with effects lasting longer than 40 min. In contrast, antiphase stimulation in the same individuals desynchronized MFC-lPFC theta phase coupling and impaired adaptive behavior. Surprisingly, the exogenously driven impairments in performance could be instantly rescued by reversing the phase angle of alternating current. The results suggest executive functions can be rapidly upor down-regulated by modulating theta phase coupling of distant frontal cortical areas and can contribute to the development of tools for potentially normalizing executive dysfunction in patient populations.high-definition transcranial alternating current stimulation | adaptive control | phase synchronization | medial frontal cortex | lateral prefrontal cortex A daptive control refers to the dynamic processing that coordinates goal pursuit, allowing us to adjust our actions to changing situations and improve performance after events such as negative feedback from the environment (1, 2). Impaired adaptive control is observed in many neurological and neuropsychiatric disorders such as schizophrenia, autism, Alzheimer's disease, attention-deficit/hyperactivity disorder, obsessivecompulsive disorder, Parkinson's disease, and epilepsy (3-9). Thus, it is not surprising that efforts to improve adaptive control have long characterized the fields of psychology and neuroscience.Computerized training has proven to be effective in the domains of language, motor function, and vision (10, 11). However, in other cognitive domains such as attention, working memory, and adaptive control, the effects of computer training interventions have been contradictory and less clear (12)(13)(14). One significant drawback to cognitive training is the duration of task practice required, often on the order of days and weeks, before desired results are achieved. Here, we asked whether it was possible to use brain stimulation technology to induce immediate and lasting neuroplastic changes in the functional connectivity hypothesized to underlie the adaptive control of behavior and learning in humans.We targeted the phase coupling or synchronization of electroencephalographic (EEG) rhythms in the ...

Changes in white matter in mice resulting from low-frequency brain stimulation

“…There is evidence that rhythmic stimulation in the theta range delivered to frontal areas can modulate behavioral performance in humans. One recent study found that 6-Hz transcranial alternating current stimulation over midline and the lateral frontal cortex improved executive function when synchronized, and reduced executive function when desynchronized (11). Many researchers have reported improved learning and performance with direct current frontal stimulation (54), although these results are mixed (55).…”

“…Moreover, human studies have provided evidence that increases in theta current density are correlated with increased metabolism in the ACC (10). When the ACC receives theta stimulation that is in phase with stimulation of a lateral frontal area, there is an improvement in measures of executive function (11). Based on these findings, we wanted to explore the potential causal relationships between increased midfrontal theta and white matter change.…”

Causal links between parietal alpha activity and spatial auditory attention

“…To correct for changes in individual performance between sessions, we referenced performance to that in the baseline block in each session. To test whether our results could be confounded by performance fluctuations in this baseline level between test days, we performed test – retest reliability analyses, comparing baseline results across different testing days 52 . We found that individual subjects’ performance across sessions were significantly correlated in both Experiment 1 (Spearman’s Rhos = 0.48; P = 0.032) and Experiment 2 (Spearman’s Rhos = 0.52; P = 0.028), indicating the stability of individual differences across testing days.…”

Multi-frequency tACS has lasting effects on neural synchrony and audiovisual responses

“…Impairment of proper coupling may lead to disorders, such as AD, PD, epilepsy, schizophrenia and autism [9]. This has fueled research into noninvasive approaches to modulate and, possibly, re-adjust neural synchrony by transcranial alternating current stimulation (tACS) [10][11][12][13][14].…”

“…In contrast, relatively little is known regarding persistent physiological effects of tACS, i.e., aftereffects on neural activity that outlast the period of electrical stimulation. Lasting modulation of intrinsic oscillations (predominantly in the alpha-band) and persistent effects on task performance or mental state have been reported in noninvasive studies [14,[24][25][26][27]. By contrast, studies addressing electrophysiological aftereffects of tACS by invasive recordings have not yet been performed.…”