Altered visual cortex excitability in premenstrual dysphoric disorder: Evidence from magnetoencephalographic gamma oscillations and perceptual suppression

Abstract

Premenstrual dysphoric disorder (PMDD) is a psychiatric condition characterized by extreme mood shifts during the luteal phase of the menstrual cycle (MC) due to abnormal sensitivity to neurosteroids and unbalanced neural excitation/inhibition (E/I) ratio. We hypothesized that in women with PMDD in the luteal phase, these factors would alter the frequency of magnetoencephalographic visual gamma oscillations, affect modulation of their power by excitatory drive, and decrease perceptual spatial suppression. Women with PMDD and control women were examined twice–during the follicular and luteal phases of their MC. We recorded visual gamma response (GR) while modulating the excitatory drive by increasing the drift rate of the high-contrast grating (static, ‘slow’, ‘medium’, and ‘fast’). Contrary to our expectations, GR frequency was not affected in women with PMDD in either phase of the MC. GR power suppression, which is normally associated with a switch from the ‘optimal’ for GR slow drift rate to the medium drift rate, was reduced in women with PMDD and was the only GR parameter that distinguished them from control participants specifically in the luteal phase and predicted severity of their premenstrual symptoms. Over and above the atypical luteal GR suppression, in both phases of the MC women with PMDD had abnormally strong GR facilitation caused by a switch from the ‘suboptimal’ static to the ‘optimal’ slow drift rate. Perceptual spatial suppression did not differ between the groups but decreased from the follicular to the luteal phase only in PMDD women. The atypical modulation of GR power suggests that neuronal excitability in the visual cortex is constitutively elevated in PMDD and that this E/I imbalance is further exacerbated during the luteal phase. However, the unaltered GR frequency does not support the hypothesis of inhibitory neuron dysfunction in PMDD.

Changes in high-frequency aperiodic 1/f slope and periodic activity reflect post-stimulus functional inhibition in the visual cortex

“…These subjects also participated in our previous study of the effect of MC on brain oscillations (V. O. Manyukhina et al, 2022). Therefore, for each individual, MEG data were collected twice, during the follicular and luteal phases, with an interval between recordings from 7 to 147 days.…”

“…We then fitted the linear function into the logarithm of the PSD vs. the logarithm of frequency using ‘polyfit’ function (Python library NumPy, v.1.21.4), the same as we did in (V.O. Manyukhina et al, 2022).…”

“…LCMV beamformer, together with the broad-band filtration in the high-frequency range, is preferable for analysis of the 35-45 Hz 1/f slope because it enables better filtering of noise and myogenic artifacts than sLORETA (V.O. Manyukhina et al, 2022). sLORETA, on the other hand, does not have depth bias in the source localization and therefore provides more realistic cortical localization of spectral power than LCMV beamformer (Tait, Özkan, Szul, & Zhang, 2021).…”

“…The aperiodic slope is steeper during ‘down states’ such as sleep and anesthesia compared to wakefulness (Colombo et al, 2019; Lendner et al, 2020; Muthukumaraswamy & Liley, 2018), during wakefulness with ‘eyes closed’ compared to ‘eyes open’ (V.O. Manyukhina et al, 2022; F. Zhang et al, 2019) and during awake states characterized by decreased information processing compared to more active states (Ouyang, Hildebrandt, Schmitz, & Herrmann, 2020; Pietrelli, Samaha, & Postle, 2022). The steepness of the aperiodic spectral slope is thought to reflect the neural E/I ratio so that a flatter (less negative) slope is associated with a higher background neuronal firing rates, decoupled from the oscillatory carrier frequency, i.e.…”

“…(V.O. Manyukhina et al, 2022; Maschke, Duclos, Owen, Jerbi, & Blain-Moraes, 2023; Ossandón et al, 2023)). In the majority of the previous studies, the aperiodic slope was estimated either in a wide frequency range, after separating the aperiodic part of the power spectral density (PSD) from the periodic activity, or at high frequencies (>30 Hz), where periodic activity is usually absent.…”