Frontoparietal Networks Mediate the Behavioral Impact of Alpha Inhibition in Visual Cortex

Abstract

Alpha oscillations are known to play a central role in the functional inhibition of visual cortices, but the mechanisms involved are poorly understood. One noninvasive method for modulating alpha activity experimentally is through the use of flickering visual stimuli that "entrain" visual cortices. Such alpha entrainment has been found to compromise visual perception and affect widespread cortical regions, but it remains unclear how the interference occurs and whether the widespread activity induced by alpha entrainment reflects a compensatory mechanism to mitigate the entrainment, or alternatively, a propagated interference signal that translates to impaired visual processing. Herein, we attempt to address these questions by integrating alpha entrainment into a modified Posner cueing paradigm, while measuring the underlying dynamics using magnetoencephalography. Our findings indicated that alpha entrainment is negatively related to task performance, such that as neural entrainment increases on the attended side (relative to the unattended side) accuracy decreases. Further, this attentional biasing is found to covary robustly with activity in the frontoparietal attention network. Critically, the observed negative entrainment effect on task accuracy was also fully mediated by activity in frontoparietal regions, signifying a propagation of the interfering alpha entrainment signal from bottom-up sensory to top-down regulatory networks.

Multi-spectral oscillatory dynamics serving directed and divided attention

“…In contrast to the theta band, we found significant effects of attention on the alpha oscillatory responses for both the directed and divided attention experiments. A widely accepted mechanism of alpha activity in the brain is the “gating by inhibition” framework ( Bonneford and Jensen, 2012 ; Hanslmayr et al, 2007 ; Händel et al, 2011 ; Jensen et al, 2002 ; Jensen and Mazaheri, 2010 ; Klimesch, 2012 ; Klimesch et al, 2007 ; Spaak et al, 2014 ; Wiesman et al, 2018 ; Wiesman and Wilson, 2019 ), whereby higher levels of alpha oscillatory activity in posterior parieto-occipital cortices index the functional inhibition of incoming visual information. Within this framework, decreases from basal levels of alpha activity represent the dis-inhibition of these cortices towards the goal of visual stimulus processing.…”

“…Neural oscillatory activity is thought to support a diverse array of neural computational functions both within and across cortical regions, and thereby may underlie numerous cognitive and behavioral processes ( Başar et al, 2001 ; Bonneford and Jensen, 2012 ; Klimesch, 1999 ; Musall et al, 2014 ; Proskovec et al, 2018a , 2019 ). Regarding visual attention, previous research using electroencephalography (EEG) and magnetoencephalography (MEG) has found alpha activity (7–13 Hz) to be central to inhibitory processing ( Bonneford and Jensen, 2012 ; Klimesch, 2012 ; McDermott et al, 2017; Proskovec et al, 2018a , 2019 ; van Dijk et al, 2008 ; Wiesman et al, 2018 ; Wiesman and Wilson, 2019 ), theta activity (3–7 Hz) to index early stimulus recognition and top-down modulatory feedback ( Basar et al, 2001 ; Busch et al, 2009 ; Klimesch et al, 2005 ; Landau and Fries, 2012 ; Landau et al, 2015 ; Proskovec et al, 2018a ; Verbruggen et al, 2010 ; Wiesman et al, 2017b ), and gamma activity (>30 Hz) to represent and possibly bind fine-grained stimulus features ( Edden et al, 2009 ; Fries et al, 2001 ; Muthukumaraswamy and Singh, 2013 ; Swettenham et al, 2009 ; Tallon-Baudry, 2009 ; Womelsdorf et al, 2006 ). Studies have also shown that inter-sensory attention reduces alpha and beta power responses to visual stimuli, as well as beta power in primary somatosensory cortex when attending to tactile stimuli ( Pomper et al, 2015 ).…”

Age-related visual dynamics in HIV-infected adults with cognitive impairment

“…Of particular interest would be studies investigating the impact of these factors on fronto-visual functional connections that are known to be formed during visuospatial attention processing. 13,14,24,[49][50][51][52] This study provides the first evidence of an interaction between age and cognitive status on neural activity in adults infected with HIV. More specifically, we found that the age-related trajectory of occipito-parietal alpha activity differs in those with HAND compared with both unimpaired HIV-infected adults and uninfected controls.…”

“…More specifically, alpha-and gamma-range neural oscillatory patterns in occipito-parietal regions were found to covary with age differently, depending on the cognitive status of the participant. Broadly, visual alpha oscillations represent the gross disinhibition of visual processing circuits, [23][24][25] whereas visual gamma activity has been implicated in more fine-tuned stimulus encoding. [26][27][28] The general pattern of these results was such that unimpaired HIV-infected adults exhibited neural dynamics more similar to the uninfected participants, whereas those with HAND exhibited markedly irregular patterns.…”

“…In the alpha band, increases in age were linked to stronger neural responses in the parieto-occipital cortices in both cognitively normal groups. Because this response indexes the usage of visuospatial resources and is modulated by attention, 23,24 this relationship should be interpreted as a compensatory recruitment of visual processing circuits as cognitively intact individuals age. In contrast, no such relationship existed in adults with HAND.…”