Neural Activity Predicts Reaction in Primates Long Before a Behavioral Response

Dezfouli, Mohsen Parto; Khamechian, Mohammad Bagher; Treue, Stefan; Esghaei, Moein; Daliri, Mohammad Reza

doi:10.3389/fnbeh.2018.00207

Cited by 13 publications

(10 citation statements)

References 47 publications

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“…This indicates that recording sites with a higher PCM showed a higher attentional modulation in the neurons recorded from them. Together with our previous observation that post-stimulus firing rate predicts reaction time 60 , our data suggest that phase coherence may influence the attentional processing of upcoming stimuli, leading to a more efficient behavior. Each time point in Fig.…”

Section: Resultssupporting

confidence: 84%

“…We hypothesize that attention shapes sensory processing by modulating inter-trial phase coherence within low frequency oscillatory activities. Given that attention enhances the behavioral detection of stimulus changes 61,62 , represented by LFPs as long as several seconds before and gamma coherence right before the response event occurs 60,63 , we asked if the modulation of phase coherence mediates the attentional influence on behavior. We conjecture that in those sets of trials with a higher phase coherence, the sensory cortex is prepared more effectively for processing sensory input, leading to a better performance in detecting stimulus changes.…”

Section: Resultsmentioning

confidence: 99%

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Attention strengthens across-trial pre-stimulus phase coherence in visual cortex, enhancing stimulus processing

Zareian

Maboudi

Daliri

et al. 2020

Sci Rep

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Attention selectively routes the most behaviorally relevant information from the stream of sensory inputs through the hierarchy of cortical areas. previous studies have shown that visual attention depends on the phase of oscillatory brain activities. these studies mainly focused on the stimulus presentation period, rather than the pre-stimulus period. Here, we hypothesize that selective attention controls the phase of oscillatory neural activities to efficiently process relevant information. We document an attentional modulation of pre-stimulus inter-trial phase coherence (a measure of deviation between instantaneous phases of trials) of low frequency local field potentials (LFP) in visual area Mt of macaque monkeys. our data reveal that phase coherence increases following a spatial cue deploying attention towards the receptive field of the recorded neural population. We further show that the attentional enhancement of phase coherence is positively correlated with the modulation of the stimulus-induced firing rate, and importantly, a higher phase coherence is associated with a faster behavioral response. these results suggest a functional utilization of intrinsic neural oscillatory activities for an enhanced processing of upcoming stimuli.One of the most important cognitive functions of the mammalian brain is selective attention. Attention selectively routes the most behaviorally relevant information from the stream of sensory inputs through the hierarchy of cortical areas. This allows the brain to make the most efficient use of its limited neural resources and to create appropriate behavioral responses quickly 1 . Attentional influences on neural responses in sensory cortex have been extensively documented; effects which reflect a multitude of aspects of cortical information processing 1-4 . Covertly directing attention towards the receptive field of a neuron in visual cortex enhances the neural responses even in the absence of visual stimulation 5,6 , alters the shape and profile of receptive fields 7-9 , modulates the variability and temporal structure of the neuron's firing patterns 10,11 , modulates inter-neuronal correlations to increase neural discriminability 12,13 and synchronizes neighboring neurons, presumably to better propagate information to downstream areas [14][15][16] .Attention has been suggested to exploit oscillatory neural activities, as well as oscillatory components of local field potentials (LFP), to enhance the efficacy of cortical processing 17-23 . LFPs represent synaptic activities of local cortical neuronal populations 24 . Their oscillations are tightly linked to attention in both low and high frequencies 18,[25][26][27][28][29] . Previous studies have shown that synchronization in the gamma as well as high gamma band

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Section: Resultssupporting

confidence: 84%

Section: Resultsmentioning

confidence: 99%

Attention strengthens across-trial pre-stimulus phase coherence in visual cortex, enhancing stimulus processing

Zareian

Maboudi

Daliri

et al. 2020

Sci Rep

Self Cite

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“…We hypothesize that attention shapes sensory processing by modulating inter-trial phase coherence within low frequency oscillatory activities. Given that attention enhances the behavioral detection of stimulus changes (Gonzalez Andino et al, 2005; Prinzmetal et al, 2005), particularly represented by LFPs as long as several seconds before the response event occurs (Parto Dezfouli et al, 2018), we asked if it is the modulation of phase coherence that underlies this attentional influence on behavior.…”

Section: Resultsmentioning

confidence: 99%

“…Esghaei et al showed that switching spatial attention to a neuron’s receptive field reduces the coupling of both gamma oscillations and spikes (both representative of local neural processing) to the low-frequency phase (Esghaei et al, 2015b; Parto Dezfouli et al, 2018) see also (Spyropoulos et al, 2018). These observations may challenge the current finding in that they suggested the coupling of local neural activity to the low frequency phase to have a suppressive role in attention.…”

Section: Discussionmentioning

confidence: 99%

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

Zareian¹,

Maboudi

et al. 2018

Preprint

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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.,...

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“…Contemporary investigations into visual areas have shown that oscillatory components of local field potential (LFP) (Liu and Newsome, 2006;Womelsdorf et al, 2006;Smith et al, 2015;Khamechian et al, 2019) and neural spiking activity (Liu and Newsome, 2005;Smith et al, 2015;Parto Dezfouli et al, 2018) could provide useful information about how neural activities are linked to visuomotor behavior. These studies have reported a trial-by-trial correlation between the power of beta (10-30 Hz) (Smith et al, 2015), gamma, and high-gamma (50-200 Hz) (Liu and Newsome, 2006) LFPs and behavioral output.…”

Section: Introductionmentioning

confidence: 99%

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

Khamechian

Daliri

2020

Front. Neurosci.

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The idea that a flexible behavior relies on synchronous neural activity within intra-and inter-associated cortical areas has been a matter of intense research in human and animal neuroscience. The neurophysiological mechanisms underlying this behavioral correlate of the synchronous activity are still unknown. It has been suggested that the strength of neural synchrony at the level of population is an important neural code to guide an efficient transformation of the sensory input into the behavioral action. In this study, we have examined the non-linear synchronization between neural ensembles in area MT of the macaque visual cortex by employing a non-linear cross-frequency coupling technique, namely bicoherence. We trained a macaque monkey to detect a brief change in the cued stimulus during a visuomotor detection task. The results show that the non-linear phase synchronization in the high-gamma frequency band (100-250 Hz) predicts the animal's reaction time. The strength of non-linear phase synchronization is selective to the target stimulus location. In addition, the non-linearity characteristics of neural synchronization are selectively modulated when the monkey covertly attends to the stimulus inside the neuron's receptive field. This additional evidence indicates that non-linear neuronal synchronization may be affected by a cognitive function like spatial attention. Our neural and behavioral observations reflect that two crucial processes may be involved in processing of visuomotor information in area MT: (I) a non-linear cortical process (measured by the bicoherence) and (II) a linear process (measured by the spectral power).

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Neural Activity Predicts Reaction in Primates Long Before a Behavioral Response

Cited by 13 publications

References 47 publications

Attention strengthens across-trial pre-stimulus phase coherence in visual cortex, enhancing stimulus processing

Attention strengthens across-trial pre-stimulus phase coherence in visual cortex, enhancing stimulus processing

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

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

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