Neuromodulation of Brain State and Behavior

McCormick, David A.; Nestvogel, Dennis; He, Biyu J.

doi:10.1146/annurev-neuro-100219-105424

Cited by 222 publications

(259 citation statements)

References 166 publications

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“…Considering these and other many studies about the influence of the low frequency ranges on diverse aspects of cognition (Baria et al, 2017;Monto et al, 2008;He, 2014;Nobre and van Ede, 2018) and the different ways that ongoing brain states modulate neural responses (Podvalny et al, 2019;McCormick et al, 2020), it is clear that part of the large variability observed in the neural responses could be explained by the ongoing, large-scale network activity and concurrent phase trajectories, and that accounting by these factors could arguably improve the capacity of MVPA to produce successful predictions.…”

Section: Discussionmentioning

confidence: 98%

Dissociable components of oscillatory activity underly information encoding in human perception

Vidaurre

Cichy

Woolrich

2020

Preprint

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Brain decoding can predict visual perception from non-invasive electrophysiological data by combining information across multiple channels. However, decoding methods typically confound together the multi-faceted and distributed neural processes underlying perception, so it is unclear what specific aspects of the neural computations involved in perception are reflected in this type of macroscale data. Using MEG data recorded while participants viewed a large number of naturalistic images, we analytically separated the brain signal into a slow 1/f drift (<5Hz) and a oscillatory response in the theta frequency band. Combined with a method for capturing between-trial variability in the way stimuli are processed, this analysis revealed that there are at least three dissociable components that contain distinct stimulus-specific information: a 1/f component, reflecting the temporally stable aspect of the stimulus representation; a global phase shift of the theta oscillation, related to differences in the speed of processing between the stimuli; and differential patterns of theta phase across channels, likely related to stimulus-specific computations. We demonstrate that common cognitive interpretations of decoding analysis can be flawed if the multicomponent nature of the signal is ignored, and suggest that, by acknowledging this fact, we can provide a more accurate interpretation of commonly observed phenomena in the study of perception.

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Section: Discussionmentioning

confidence: 98%

Dissociable components of oscillatory activity underly information encoding in human perception

Vidaurre

Cichy

Woolrich

2020

Preprint

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“…Cortical states can vary over a wide range and have been shown to be in a tight relationship with many functions that are relevant to psychiatric disorders, such as arousal level, perceptual ability, cognitive task engagement, and reaction times. It is thus no surprise that there have been longstanding efforts to understand the neural factors contributing to cortical state fluctuations (Harris and Thiele, 2011;McGinley et al, 2015;McCormick et al, 2020). While the LC has been long implicated in having a role in determining cortical state maintenance and transitions, LC neuronal population activity has always been thought and shown to produce a single activated cortical state (similar to that observed in sleep-wake transitions) by presumably collective firing of the LC neurons (Carter et al, 2010;Marzo et al, 2014;Hayat et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…Flexible behavior is associated with transitions across diverse cortical states. For example, various states of wakefulness, perceptual ability, and behavioral activity are associated with different cortical states each with its own clear pattern of neural oscillations and synchronization properties (Harris and Thiele, 2011;McGinley et al, 2015;McCormick et al, 2020). Moreover, behavioral state transitions, such as waking from sleep or entering a state of heightened stress and reacting more quickly to stimuli, are associated with cortical state transition.…”

Section: Introductionmentioning

confidence: 99%

Distinct ensembles in the noradrenergic locus coeruleus evoke diverse cortical states

Noei

Zouridis

Logothetis

et al. 2020

Preprint

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13Identifying the neurons that control global brain state has been a fundamental topic of research 14 that has largely focused on diffusely-projecting neuromodulatory centers, such as the locus 15 coeruleus (LC). This noradrenergic brain stem nucleus, which projects throughout the forebrain, 16 is thought to act as an "undifferentiated state controller" across all forebrain targets because LC 17 neurons spike synchronously. However, recent work demonstrated ensembles in the LC and 18 therefore made targeted neuromodulation a possibility. In order to demonstrate that LC 19 ensembles cause targeted neuromodulation, it is necessary to resolve LC ensemble dynamics 20 over time in relation to ongoing cortical states. Here, we used non-negative matrix factorization 21 on LC single unit recordings to investigate the spatial and temporal properties of ensemble 22 activation patterns. We assessed the potential for targeted neuromodulation of the prefrontal 23 cortex (PFC) using LC ensemble activity-triggered local field potential (LFP) power spectrograms. 24We analyzed 285 single units recorded from 15 urethane-anesthetized rats (range of 5 to 34 25 simultaneously recorded units). LC ensembles became active at different times. Analysis of auto-26 correlograms and ensemble-pair cross-correlograms demonstrated that self-and lateral-inhibition 27 of activity is a property of LC ensembles, which may contribute to their sparse activity. 28Neuromodulatory effects on cortical state were diverse across ensembles. We observed four 29 types of ensemble-triggered LFP spectrograms in the PFC. These results demonstrate that the 30 LC is capable of differentiated neuromodulation of its forebrain targets by dynamic firing patterns 31 across subsets of LC neurons. 34Internal, spontaneously occurring brain states are associated with changes in wakefulness, 35perceptual ability, and reaction times (1-3). Behavioral transitions, such as waking from sleep or 36 reacting more quickly to stimuli during stress, involve changes in global brain state. It remains 37 unclear exactly which neurons could control brain state globally. 38Brainstem neuromodulatory centers, such as the noradrenergic locus coeruleus (LC), are a likely 39 global state-controller (1, 2, 4). The LC projects globally throughout the central nervous system 40 and releases norepinephrine to modulate neuronal excitability (5-11). Global noradrenergic 41 neuromodulation can result in behavioral transitions, such as: awakening from sleep or 42 anesthesia, altering locomotion patterns (increased generalized movements and decreased 43 reaction times), and improving perceptual sensitivity and attentional focus (12-24). The brain 44 state change that occurs spontaneously during behavioral transitions, such as awakening, also 45 resembles the brain state evoked by stimulation of the LC in awake or anesthetized animals (9, 46 16, 24, 25). Thus, the LC is thought to be at least one group of neurons that can alter global brain 47 states associated with behavioral state transitions. 48 LC n...

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confidence: 99%

Phasic activation of dorsal raphe serotonergic neurons increases pupil-linked arousal

Cazettes

Reato

Morais

et al. 2020

Preprint

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Variations in pupil size under constant luminance are closely coupled to changes in arousal state [1][2][3][4][5]. It is assumed that such fluctuations are primarily controlled by the noradrenergic system [6][7][8][9]. Phasic activity of noradrenergic axons precedes pupil dilations associated with rapid changes in arousal [7,9], and is believed to be driven by unexpected uncertainty [1,[10][11][12][13][14][15][16]. However, the role of other modulatory pathways in the control of pupil-linked arousal has not been as thoroughly investigated, but evidence suggests that noradrenaline may not be alone [7,17,18]. Administration of serotonergic drugs seems to affect pupil size [19][20][21][22][23], but these effects have not been investigated in detail. Here, we show that transient serotonin (5-HT) activation, like noradrenaline, causes pupil-size changes. We used phasic optogenetic activation of 5-HT neurons in the dorsal raphe nucleus (DRN) in head-fixed mice locomoting in a foraging task. 5-HT-driven modulations of pupil size were maintained throughout the photostimulation period and sustained for several seconds after the end of the stimulation. The activation of 5-HT neurons increased pupil size additively with locomotor speed, suggesting that 5-HT transients affect pupil-linked arousal independently from locomotor states. We found that the effect of 5-HT on pupil size depended on the level of environmental uncertainty, consistent with the idea that 5-HT may report a salience or surprise signal [24] . Together, these results challenge the classic view of the neuromodulatory control of pupil-linked arousal, revealing a tight relationship between the activation of 5-HT neurons and changes in pupil size.

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Neuromodulation of Brain State and Behavior

Cited by 222 publications

References 166 publications

Dissociable components of oscillatory activity underly information encoding in human perception

Dissociable components of oscillatory activity underly information encoding in human perception

Distinct ensembles in the noradrenergic locus coeruleus evoke diverse cortical states

Phasic activation of dorsal raphe serotonergic neurons increases pupil-linked arousal

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