Regular recreational Cannabis users exhibit altered neural oscillatory dynamics during attention reorientation

Abstract

Background Cannabis is the most widely used illicit drug in the United States and is often associated with changes in attention function, which may ultimately impact numerous other cognitive faculties (e.g. memory, executive function). Importantly, despite the increasing rates of cannabis use and widespread legalization in the United States, the neural mechanisms underlying attentional dysfunction in chronic users are poorly understood. Methods We used magnetoencephalography (MEG) and a modified Posner cueing task in 21 regular cannabis users and 32 demographically matched non-user controls. MEG data were imaged in the time−frequency domain using a beamformer and peak voxel time series were extracted to quantify the oscillatory dynamics underlying use-related aberrations in attentional reorienting, as well as the impact on spontaneous neural activity immediately preceding stimulus onset. Results Behavioral performance on the task (e.g. reaction time) was similar between regular cannabis users and non-user controls. However, the neural data indicated robust theta-band synchronizations across a distributed network during attentional reorienting, with activity in the bilateral inferior frontal gyri being markedly stronger in users relative to controls (p's < 0.036). Additionally, we observed significantly reduced spontaneous theta activity across this distributed network during the pre-stimulus baseline in cannabis users relative to controls (p's < 0.020). Conclusions Despite similar performance on the task, we observed specific alterations in the neural dynamics serving attentional reorienting in regular cannabis users compared to controls. These data suggest that regular cannabis users may employ compensatory processing in the prefrontal cortices to efficiently reorient their attention relative to non-user controls.

Regular cannabis use modulates the impact of HIV on the neural dynamics serving cognitive control

“…Finally, we also found that the association between the strength of spontaneous baseline activity and neural oscillations in the same spectral band was stronger in the dlPFC of cannabis users relative to nonusers, which may indicate that cannabis users are better able to compensate through increased oscillatory strength. These findings are consistent with previous literature that suggests both spontaneous and oscillatory power are altered in regular cannabis users (Edwards et al, 2009; Springer et al, 2021), and that cannabis use in PWH may have a neuroprotective effect, at least in some brain regions (Christopher-Hayes et al, 2021; Hall et al, 2021; Meade et al, 2016).…”

“…compensate through increased oscillatory strength. These findings are consistent with previous literature that suggests both spontaneous and oscillatory power are altered in regular cannabis users (Edwards et al, 2009;Springer et al, 2021), and that cannabis use in PWH may have a neuroprotective effect, at least in some brain regions (Christopher-Hayes et al, 2021;Hall et al, 2021;Meade et al, 2016).…”

“…Cognitive impairments are thought to arise from dysregulated dopaminergic signaling resulting from an excitatory/inhibitory imbalance due to a reduction in GABAergic inhibitory inputs in the PFC, thus leading to diminished pyramidal cell firing synchrony between neurons in the hippocampus and PFC (Paspalas and Goldman-Rakic, 2005; Skosnik et al, 2016). Studies using MEG and EEG have shown that regular cannabis use is associated with local decreases in power, both at rest and during task performance (Christopher-Hayes et al, 2021; Edwards et al, 2009; Herning et al, 2003; Rangel-Pacheco et al, 2021; Springer et al, 2021). In fact, one study found that those with greater cannabis exposure had the lowest spectral power, and these findings were more pronounced in frontal regions of the brain (Edwards et al, 2009).…”

“…Despite this, several studies have found decreased activation in regular cannabis users relative to nonusers in regions such as the PFC and parietal cortices and in the medial cerebellum during cognitive control tasks (Abdullaev et al, 2010; Chang et al, 2006). In addition, MEG studies of cognitive control and attentional reorientation have found that regular cannabis users have aberrant theta interference responses in the right occipital cortex, altered theta fronto-occipital functional connectivity, and weaker spontaneous and stronger oscillatory theta activity in the inferior frontal gyri, suggesting that cannabis users employ compensatory neural processing during higher-order cognitive tasks (Rangel-Pacheco et al, 2021; Springer et al, 2021).…”

Occipital neural dynamics in cannabis and alcohol use: independent effects of addiction

“…However, our study did not assess oscillatory activity in the context of short-term drug effects, and such acute effects of cannabis are unlikely to generalize to our sample of chronic users who had not recently consumed such substances. Still other studies have identified alterations in chronic cannabis users in oscillatory activity related to attentional processing 45,46 . Compared to these studies however, the current study utilized a paradigm that did not utilize an attentional comparison.…”