Cannabis use impacts pre-stimulus neural activity in the visual cortices of people with HIV

Abstract

People with HIV (PWH) use cannabis at a higher rate than the general population, but the influence on neural activity is not well characterized. Cannabis use among PWH may have a beneficial effect, as neuroinflammation is known to be a critical problem in PWH and cannabis use has been associated with a reduction in proinflammatory markers. Thus, it is important to understand the net impact of cannabis use on brain and cognitive function in PWH. In this study, we collected magnetoencephalographic (MEG) brain imaging data on 81 participants split across four demographically matched groups (i.e., PWH using cannabis, controls using cannabis, non-using PWH, and non-using controls). Participants completed a visuospatial processing task during MEG. Time-frequency resolved voxel time series were extracted to identify the dynamics of oscillatory and pre-stimulus baseline neural activity. Our results indicated strong theta (4-8 Hz), alpha (10-16 Hz), and gamma (62-72 Hz) visual oscillations in parietal-occipital brain regions across all participants. PWH exhibited significant behavioral deficits in visuospatial processing, as well as reduced theta oscillations and elevated pre-stimulus gamma activity in visual cortices, all of which replicate prior work. Strikingly, chronic cannabis use was associated with a significant reduction in pre-stimulus gamma activity in the visual cortices, such that PWH no longer statistically differed from controls. These results provide initial evidence that cannabis use may normalize some neural aberrations in PWH. This study fills an important gap in understanding the impact of cannabis use on brain and cognitive function in PWH.

Keywords: MEG; gamma; magnetoencephalography; neural oscillations; neurocognitive decline; visuospatial processing.

FIGURE 1

Experimental paradigm and behavioral results. (a) An illustration of the visuospatial task paradigm. Each trial was comprised of a fixation period lasting 2,000 ms (variable interstimulus interval: 1,900–2,100 ms) and a stimulus‐presentation period lasting 800 ms, which consisted of the appearance of a checkered grid in one of four locations. (b) Behavioral results from the visuospatial task; reaction time (in ms) is displayed on the y‐axis of the graph on the left, and accuracy (in % correct) is displayed on the y‐axis of the graph to the right. The color legend is shown to the far right (*p < .01)

FIGURE 2

Neural responses serving visuospatial processing. (a): Spectrograms showing the three oscillatory responses identified at the MEG sensor level. Time (in ms) is denoted on the x‐axes, with 0 ms defined as the onset of the visual stimulus, and frequency (in Hz) is shown on the y‐axes. The lower spectrogram shows the theta (4–8 Hz, 25–275 ms) and alpha (8–14 Hz, 200–600 ms) responses, while the upper spectrogram shows the gamma (68–74 Hz, 200–600 ms) response. Insets show 2D power topographies of each oscillatory response grand‐averaged across the time–frequency windows of interest. (b): Activity from volumetric source images projected to the surface for visualization. Rows from top to bottom represent neural responses within the time and spectral windows of interest (i.e., gamma, alpha, theta). The color scale bars for spectrograms and 2D topographies (to the right of each plot), and for source maps (bottom of each plot) for each response reflects baseline‐normalized changes in power from the pre‐stimulus period

FIGURE 3

Oscillatory theta responses during visuospatial processing are weaker in PWH. (Left column): Time series from the peak voxel per oscillatory response collapsed across left and right hemispheric peaks in each participant and group averaged for visualization. The line features indicate group (legend on far right) and the gray highlighted area indicates the active window used to compute the means shown in the right column. In each plot, time (ms) is denoted on the x‐axis, with 0 ms defined as the onset of the visual stimulus, and the relative amplitude (in % from baseline) is denoted on the y‐axis. The inset shows functional images and location of peak voxel for improved clarity. (Right column): The means of each group computed from the gray highlighted area in the time series shown in the left column. Participant group is denoted via both the x‐axis and hue (*p < .05)

FIGURE 4

Gamma‐band neural activity was elevated in PWH and decreased in cannabis users. (Left column): Absolute amplitude time series from the same voxels shown in Figure 4 have been collapsed across hemisphere in each participant and group averaged for display. Line features indicate group and the gray highlighted area indicates the window of interest for computing neural activity during the baseline. Time (in ms) is denoted on the x‐axis, with 0 ms defined as the onset of the visual stimulus, and absolute amplitude (in nAm) is denoted on the y‐axis. The inset shows the location of the peak‐voxels. (Right column): The means of each group computed from the gray highlighted area in the left column per response. Participant group is denoted via both the x‐axis and hue. (a) Pre‐stimulus theta and alpha activity were not significantly affected by HIV or cannabis use, while (b) Pre‐stimulus gamma activity was affected by both. (*p < .05; **p < .001)