Dynamics of the functional link between area MT LFPs and motion detection

Abstract

-The evolution of a visually guided perceptual decision results from multiple neural processes, and recent work suggests that signals with different neural origins are reflected in separate frequency bands of the cortical local field potential (LFP). Spike activity and LFPs in the middle temporal area (MT) have a functional link with the perception of motion stimuli (referred to as neural-behavioral correlation). To cast light on the different neural origins that underlie this functional link, we compared the temporal dynamics of the neural-behavioral correlations of MT spikes and LFPs. Wide-band activity was simultaneously recorded from two locations of MT from monkeys performing a threshold, two-stimuli, motion pulse detection task. Shortly after the motion pulse occurred, we found that high-gamma (100 -200 Hz) LFPs had a fast, positive correlation with detection performance that was similar to that of the spike response. Beta (10 -30 Hz) LFPs were negatively correlated with detection performance, but their dynamics were much slower, peaked late, and did not depend on stimulus configuration or reaction time. A late change in the correlation of all LFPs across the two recording electrodes suggests that a common input arrived at both MT locations prior to the behavioral response. Our results support a framework in which early high-gamma LFPs likely reflected fast, bottom-up, sensory processing that was causally linked to perception of the motion pulse. In comparison, late-arriving beta and highgamma LFPs likely reflected slower, top-down, sources of neuralbehavioral correlation that originated after the perception of the motion pulse.behavior; cortex; local field potential; MT; vision VISUALLY GUIDED DECISIONS involve multiple neural components, such as sensory and evaluative stages (Gold and Shadlen 2007). But when and how do different neural components make their contribution? This question is typically studied by measuring the trial-by-trial correlation between cortical spiking and perceptual behavior (Parker and Newsome 1998). Interpreting these neural-behavioral correlations, however, is difficult because they do not tell us whether fluctuations in neural activity directly produced fluctuations in perception. Thus additional data are needed to better understand and model the causality behind observed neural-behavioral correlations.Recent efforts have focused on the local field potential (LFP) and suggest that distinct neurophysiological processes can be measured from different LFP frequency bands (Bastos et al. 2015;Katzner et al. 2009;Kopell et al. 2010;Siegel et al. 2012). Gamma-band LFPs are thought to carry stimulus information (Belitski et al. 2010) and reflect the synaptic inputs from earlier stages (Khawaja et al. 2009) and the activity of local neurons (Ray and Maunsell 2011a), while beta-band LFPs may reflect intercortical feedback (Saalmann et al. 2007). Correspondingly, attention increases gamma LFP power in a manner similar to that of local spiking activity, while beta power is attenuated (Khaya...

Neural Activity Predicts Reaction in Primates Long Before a Behavioral Response

“…How neural activities control the behavior (either choice or performance) is a crucial question in neuroscience. Previous studies have reported a link between behavioral performance and the neural activity in different brain areas, such as the trigeminothalamic system (Maixner et al, 1989 ; Bushnell et al, 1993 ), the somatosensory system (Sinclair and Burton, 1991 ; Romo et al, 1996 ), superior colliculus (Horwitz and Newsome, 2001 ) and visual cortex (Newsome et al, 1989 ; Britten et al, 1996 ; Shadlen et al, 1996 ; Horwitz and Newsome, 2001 ; Cook and Maunsell, 2002 ; Barberini et al, 2005 ; Liu and Newsome, 2005 , 2006 ; Cohen and Newsome, 2009 ; Cohen and Maunsell, 2010 ; Kajikawa and Schroeder, 2011 ; van Ede et al, 2012 ; Smith et al, 2015 ). Additionally, it has been reported that behavioral choice is closely connected to the neural activity (Johansson and Vallbo, 1979 ; Newsome et al, 1989 ; Bushnell et al, 1993 ; Britten et al, 1996 ; Romo et al, 1996 ; Shadlen et al, 1996 ; Horwitz and Newsome, 2001 ; Cook and Maunsell, 2002 ; Barberini et al, 2005 ; Liu and Newsome, 2005 , 2006 ).…”

Routing information flow by separate neural synchrony frequencies allows for “functionally labeled lines” in higher primate cortex

“…Complex neural tasks such as converting sensory information into appropriate motor actions and the associated decision processes require carefully and dynamically coordinated neural activity in networks of cortical areas (1–5). Many studies have shown that the response variability of the contributing populations of sensory neurons play a central role in determining the variations of behavioral response (6–18), as well as perceptual decisions (19–21). Local field potentials (LFPs)—signals representing the extracellular neural activity in a local volume of brain tissue—provide a measure for activities mediated by relatively localized neuronal pools (22, 23).…”

“…These signals, extracted from the low-frequency (<500 Hz) components of extracellular neural signals, reflect mainly the collective synaptic activities across local neural populations (23, 24), predominantly induced by the local spiking activity (25). Recent research has shown that LFP signals could provide useful information on how neural activities are linked to behavior (12, 14, 16, 17, 26). These studies have demonstrated that the power of gamma and high-gamma (50 to 200 Hz) LFPs, as well as multiunit neural activities, in area MT of primate visual cortex are linked to behavioral outputs in a trial-by-trial manner (14, 16).…”

“…Recent research has shown that LFP signals could provide useful information on how neural activities are linked to behavior (12, 14, 16, 17, 26). These studies have demonstrated that the power of gamma and high-gamma (50 to 200 Hz) LFPs, as well as multiunit neural activities, in area MT of primate visual cortex are linked to behavioral outputs in a trial-by-trial manner (14, 16). Moreover, the strength of gamma synchrony induced among MT neurons reflects the size of correlation between neural activity and behavior (12).…”

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

“…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. Moreover, they have shown that the strength of gamma (Womelsdorf et al, 2006) and high-gamma synchronization (Khamechian et al, 2019) between sensory neurons in the dorsal and ventral visual pathway, respectively, predict the speed of behavioral responses.…”