Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention

Spooner, Rachel K.; Wiesman, Alex I.; Proskovec, Amy L.; Heinrichs‐Graham, Elizabeth; Wilson, Tony W.

doi:10.1002/hbm.24819

Cited by 34 publications

(25 citation statements)

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“…Specifically, we found that theta oscillatory responses (i.e., synchronizations) were largely equivalent during valid and invalid trials in younger controls, but with increasing age the difference between the two (i.e., the validity effect) increased, with invalid trials being associated with stronger theta responses. Previous studies have repeatedly tied prefrontal theta activity to attentional reorienting towards goal-relevant stimuli [53,98,99] and its modulation with ageing [100,101], and thus these results are congruent with previous reports. In contrast, PWH exhibited a different trajectory of prefrontal theta activity with increasing age, as young PWH showed stronger theta responses on invalid relative to valid trials, but with increasing age this pattern reversed and PWH responded equally or slightly more strongly to valid trials.…”

Section: Discussionsupporting

confidence: 90%

The age-related trajectory of visual attention neural function is altered in adults living with HIV: A cross-sectional MEG study

et al. 2020

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Background Despite living a normal lifespan, at least 35% of persons with HIV (PWH) in resource-rich countries develop HIV-associated neurocognitive disorder (HAND). This high prevalence of cognitive decline may reflect accelerated ageing in PWH, but the evidence supporting an altered ageing phenotype in PWH has been mixed. Methods We examined the impact of ageing on the orienting of visual attention in PWH using dynamic functional mapping with magnetoencephalography (MEG) in 173 participants age 22–72 years-old (94 uninfected controls, 51 cognitively-unimpaired PWH, and 28 with HAND). All MEG data were imaged using a state-of-the-art beamforming approach and neural oscillatory responses during attentional orienting were examined for ageing, HIV, and cognitive status effects. Findings All participants responded slower during trials that required attentional reorienting. Our functional mapping results revealed HIV-by-age interactions in left prefrontal theta activity, alpha oscillations in the left parietal, right cuneus, and right frontal eye-fields, and left dorsolateral prefrontal beta activity ( p <.005). Critically, within PWH, we observed a cognitive status-by-age interaction, which revealed that ageing impacted the oscillatory gamma activity serving attentional reorienting differently in cognitively-normal PWH relative to those with HAND in the left temporoparietal, inferior frontal gyrus, and right prefrontal cortices ( p <.005). Interpretation This study provides key evidence supporting altered ageing trajectories across vital attention circuitry in PWH, and further suggests that those with HAND exhibit unique age-related changes in the oscillatory dynamics serving attention function. Additionally, our neural findings suggest that age-related changes in PWH may serve a compensatory function. Funding National Institutes of Health, USA.

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Section: Discussionsupporting

confidence: 90%

The age-related trajectory of visual attention neural function is altered in adults living with HIV: A cross-sectional MEG study

et al. 2020

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“…The engagement of motor gamma oscillations in this situation speak of mechanisms oriented to process the dynamic and uncertain conditions of our environment. These findings converge with other studies that show the responsiveness of motor gamma activity to environmental cues, such as in attentional capture ( Spooner et al, 2020 ). This responsiveness to dynamical environmental demands highlights the adaptive functions that motor gamma oscillations have and its potential implications for our interactions with our surrounding environment.…”

Section: Motor Gamma Oscillationssupporting

confidence: 92%

The Control of Movements via Motor Gamma Oscillations

Ulloa

2022

Front. Hum. Neurosci.

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The ability to perform movements is vital for our daily life. Our actions are embedded in a complex environment where we need to deal efficiently in the face of unforeseen events. Neural oscillations play an important role in basic sensorimotor processes related to the execution and preparation of movements. In this review, I will describe the state of the art regarding the role of motor gamma oscillations in the control of movements. Experimental evidence from electrophysiological studies has shown that motor gamma oscillations accomplish a range of functions in motor control beyond merely signaling the execution of movements. However, these additional aspects associated with motor gamma oscillation remain to be fully clarified. Future work on different spatial, temporal and spectral scales is required to further understand the implications of gamma oscillations in motor control.

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“…Other spectral changes involved in motor control include low (i.e., theta) and high (i.e., gamma) frequency oscillations that occur during movement onset and importantly may serve as temporal coordinators ( 61 , 62 ) or execution signals for volitional movement ( 33 , 63 , 64 ), respectively. Although recent work has also demonstrated that such gamma oscillations are modulated by higher-order processes such as response interference and attentional reorienting ( 65 – 69 ). While the current study focused on the impact of the mitochondrial redox environment on peri-movement beta responses due to their established relationship with behavior ( 1 – 4 , 8 , 9 , 11 , 43 , 60 , 69 ), we did probe the other oscillatory responses in our supplementary analyses and found that the effects were generally specific to beta oscillations during motor planning and execution.…”

Section: Discussionmentioning

confidence: 99%

“…Note that the significant time–frequency extent of the peri-movement beta response extended beyond this 1,000-ms period. Further details of our MEG data processing pipeline can be found in recent manuscripts ( 43 , 68 , 69 , 73 ).…”

Section: Methodsmentioning

confidence: 99%

Neural oscillatory activity serving sensorimotor control is predicted by superoxide-sensitive mitochondrial redox environments

Spooner

Taylor

Ahmad

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Significance Mitochondrial integrity and associated redox profiles have long been revered as key contributors to a host of age- and disease-related pathologies, which eventually lead to neuronal and behavioral dysfunction in the sensorimotor and other systems. However, the precise role of the mitochondrial redox environment in human sensorimotor brain systems and motor behavior remains poorly understood. Herein, we provide evidence for a strong predictive capacity of superoxide and its scavenger, superoxide dismutase, on the neural oscillatory dynamics serving motor planning and execution above and beyond the effects of mitochondrial respiratory capacities alone. Importantly, these data provide insight regarding the impact of the redox environment on the population-level neural oscillations that serve motor function in healthy humans.

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Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention

Cited by 34 publications

References 50 publications

The age-related trajectory of visual attention neural function is altered in adults living with HIV: A cross-sectional MEG study

The age-related trajectory of visual attention neural function is altered in adults living with HIV: A cross-sectional MEG study

The Control of Movements via Motor Gamma Oscillations

Neural oscillatory activity serving sensorimotor control is predicted by superoxide-sensitive mitochondrial redox environments

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