Attention enhances LFP phase coherence in macaque visual cortex, improving sensory processing

Abstract

24Attention selectively routes the most behaviorally relevant information among the vast 25 pool of sensory inputs through cortical regions. Previous studies have shown that visual 26 attention samples the surrounding stimuli periodically. However, the neural mechanism 27 underlying this sampling in the sensory cortex, and whether the brain actively uses these 28 rhythms, has remained elusive. Here, we hypothesize that selective attention controls the 29 phase of oscillatory synaptic activities to efficiently process the relevant information in 30 the brain. We document an attentional modulation of pre-stimulus inter-trial phase 31 coherence (a measure of deviation between instantaneous phases of trials) at low 32 frequencies in macaque visual area MT. Our data reveal that phase coherence increases 33 when attention is deployed towards the receptive field of the recorded neural population. 34 We further show that the attentional enhancement of phase coherence is positively 35 correlated with the attentional modulation of stimulus induced firing rate, and 36 importantly, a higher phase coherence leads to a faster behavioral response. Our results 37 suggest a functional utilization of intrinsic neural oscillatory activities for better 38 processing upcoming environmental stimuli, generating the optimal behavior. 39 attention | local field potentials | phase coherence | reaction time | visual cortex 40 41 72 (Yamagishi et al., 2003). Although there is prominent evidence on attentional modulation of 73 low frequency amplitude, the role of low frequency phase in attentional processing is yet 74 controversial. 75 The phase of low frequency oscillations modulates local neural activities represented by 76 gamma band activity, which presumably enables distant brain regions to interact (Demiralp et 77 al. , 2007). Some studies have shown that the phase of ongoing neural oscillations is responsible 78 for periodic sampling by visual attention (Busch and VanRullen, 2010; VanRullen et al., 2011). 79Furthermore, the phase of low frequency oscillations facilitates information transfer and neural 80 coding in the brain (Voloh and Womelsdorf, 2016). Therefore, low frequency phase can enable 81 the neural system to prepare for processing upcoming sensory stimuli. 82Pre-stimulus neural activity has been shown to be a determinant of retrieving episodic memory, 83 perception of environmental information and attention-related variability in response speed 84 (Addante et al., 2011; Hanslmayr et al., 2013 Hanslmayr et al., , 2007 Shibata et al., 2008). Interestingly, it has 85 been shown that pre-stimulus brain activity causally determines visual perception (Dugué et 86 al., 2011). In addition, it has been shown that the phase of low frequency oscillations is 87 responsible for this causal relationship (Hanslmayr et al., 2013). Furthermore, attention has 88 been reported to determine the phase of low frequency neural oscillations in order to influence 89 neuronal responses and behavioral responses to external events (Lakatos et al.,...

Decoding Adaptive Visuomotor Behavior Mediated by Non-linear Phase Coupling in Macaque Area MT

“…We speculate that this finding is possibly due to the influence of a cognitive function like attention that enhances the non-linear synchronization between local neurons. Our hypothesis is in line with previous studies that have shown that spatial attention selectively increases the strength of synchronization between neurons processing the target stimulus (Womelsdorf et al, 2006;Zareian et al, 2018;Khamechian et al, 2019).…”

STN-PFC circuit related to attentional fluctuations during non-movement decision-making

“…In our study, we found STN activ covaried with attentional fluctuation, too. ITPC in the STN during correct trials is significantly lo than during incorrect trials across theta, alpha, and beta bands, in line with previous brain-compu interface (BCI) paradigms in EEG (Zareian et al, 2020). The theta-BHG coupling in prefrontal regi and STN was also covaried with attentional fluctuation.…”

“…Some researchers investigate the effect of attention on inter-trial phase coherence at pre-stimulus low-frequency oscillations in area MT of monkey. Their results reveal that phase coherence in theta band increases when attention is deployed towards the receptive field of the recorded neuron (Zareian et al, 2020). In our study, we compared inter-trial phase coherence (ITPC) between the correct and incorrect trials in frontal regions and STN (Fig.…”

Attentional brain rhythms during prolonged cognitive activity

“…Second, we show that on high behavioral performance epochs, LFP alpha coherency is higher than on low behavioral performance epochs. Signal coherency within and between brain areas is proposed as a key mechanism at the core of brain computing functions and supports information/stimulus processing(Fries, 2015b), accounting for network connectivity(Vinck et al, 2010), and changes in behavioral performance(Zareian et al, 2018, 2020). Last, we report changes in spike field coherency within the prefrontal cortex between the epochs of high vs. low behavioral performance, in the same frequency ranges as reported by others during attention orientation(Fries et al, 2008; Gregoriou et al, 2009b; Paneri and Gregoriou, 2017), thus pointing to a direct modulation of attentional mechanisms.…”