Theta and Alpha Oscillatory Activity During Working Memory Maintenance in Long-Term Cannabis Users: The Importance of the Polydrug Use Context

Abstract

Background: Impairments in various subdomains of memory have been associated with chronic cannabis use, but less is known about their neural underpinnings, especially in the domain of the brain’s oscillatory activity.Aims: To investigate neural oscillatory activity supporting working memory (WM) in regular cannabis users and non-using controls. We focused our analyses on frontal midline theta and posterior alpha asymmetry as oscillatory fingerprints for the WM’s maintenance process.Methods: 30 non-using controls (CG) and 57 regular cannabis users—27 exclusive cannabis users (CU) and 30 polydrug cannabis users (PU) completed a Sternberg modified WM task with a concurrent electroencephalography recording. Theta, alpha and beta frequency bands were examined during WM maintenance.Results: When compared to non-using controls, the PU group displayed increased frontal midline theta (FMT) power during WM maintenance, which was positively correlated with RT. The posterior alpha asymmetry during the maintenance phase, on the other hand, was negatively correlated with RT in the CU group. WM performance did not differ between groups.Conclusions: Both groups of cannabis users (CU and PU), when compared to the control group, displayed differences in oscillatory activity during WM maintenance, unique for each group (in CU posterior alpha and in PU FMT correlated with performance). We interpret those differences as a reflection of compensatory strategies, as there were no differences between groups in task performance. Understanding the psychophysiological processes in regular cannabis users may provide insight on how chronic use may affect neural networks underlying cognitive processes, however, a polydrug use context (i.e., combining cannabis with other illegal substances) seems to be an important factor.

The neural oscillations serving task switching are altered in cannabis users

“…Furthermore, differences in theta activity have been repeatedly reported in neuroimaging studies comparing cannabis users and nonusers (Binkowska et al, 2021; Rangel-Pacheco et al, 2021; Springer et al, 2023). For example, in working memory and attention-reorientation tasks, cannabis users have been shown to exhibit stronger theta activity in the PFC and inferior frontal gyrus, respectively, relative to nonusers (Binkowska et al, 2021; Springer et al, 2023).…”

“…Furthermore, differences in theta activity have been repeatedly reported in neuroimaging studies comparing cannabis users and nonusers (Binkowska et al, 2021;Rangel-Pacheco et al, 2021;Springer et al, 2023). For example, in working memory and attention-reorientation tasks, cannabis users have been shown to exhibit stronger theta activity in the PFC and inferior frontal gyrus, respectively, relative to nonusers (Binkowska et al, 2021;Springer et al, 2023). By contrast, we found significantly weaker theta switch cost responses in cannabis users relative to nonusers, although it is important to note that switch cost maps are derived from the neural response profile across two conditions.…”

“…For example, an imaging study examining the effects of binge drinking on frontal activation during an inhibitory control task found that decreased dmPFC and dlPFC activation were associated with greater recent binge drinking (Cohen-Gilbert et al, 2017). Furthermore, differences in theta activity have been repeatedly reported in neuroimaging studies comparing cannabis users and nonusers (Binkowska et al, 2021;Rangel-Pacheco et al, 2021;Springer et al, 2023). For example, in working memory and attention-reorientation tasks, cannabis users have been shown to exhibit stronger theta activity in the PFC and inferior frontal gyrus, respectively, relative to nonusers (Binkowska et al, 2021;Springer et al, 2023).…”

“…Fourth, we did not examine the acute effects of cannabis consumption, as all participants abstained from use prior to the study visit. EEG research has suggested that acute cannabis administration is associated with a decrease in theta power during a working memory task (Binkowska et al, 2021). Future work should examine oscillatory activity during the acute intoxication phase to quantify the differential effects of acute and chronic cannabis use on the neural oscillatory dynamics serving cognitive flexibility.…”