Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms

Buzsáki, György; Logothetis, Nikos K.; Singer, Wolf

doi:10.1016/j.neuron.2013.10.002

Cited by 779 publications

(751 citation statements)

References 154 publications

(183 reference statements)

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“…Such temporal characteristics indicate that the brain-wide integration of spiking information from multiple thalamic neurons simultaneously, possibly through bursting activity, requires extended time windows. These interactions presumably synchronize remote brain regions that require large conduction delays (19)(20)(21).…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies integrating large-scale electrical recordings, voltage-sensitive dye (VSD), and Ca 2+ -imaging techniques (15-18) support the hypothesis that slow, oscillating neural activity constrains and elicits these hemodynamic fluctuations. Furthermore, low-frequency activity can temporally synchronize remote brain regions for extended periods to enable information processing (19)(20)(21). Although studies demonstrated that rsfMRI connectivity is constrained by well-defined structural networks (3, 17), connectivity itself can reorganize during learning-related tasks (22).…”

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confidence: 99%

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Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Leong

Chan

Gao

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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One challenge in contemporary neuroscience is to achieve an integrated understanding of the large-scale brain-wide interactions, particularly the spatiotemporal patterns of neural activity that give rise to functions and behavior. At present, little is known about the spatiotemporal properties of long-range neuronal networks. We examined brain-wide neural activity patterns elicited by stimulating ventral posteromedial (VPM) thalamo-cortical excitatory neurons through combined optogenetic stimulation and functional MRI (fMRI). We detected robust optogenetically evoked fMRI activation bilaterally in primary visual, somatosensory, and auditory cortices at low (1 Hz) but not high frequencies (5-40 Hz). Subsequent electrophysiological recordings indicated interactions over long temporal windows across thalamo-cortical, cortico-cortical, and interhemispheric callosal projections at low frequencies. We further observed enhanced visually evoked fMRI activation during and after VPM stimulation in the superior colliculus, indicating that visual processing was subcortically modulated by low-frequency activity originating from VPM. Stimulating posteromedial complex thalamo-cortical excitatory neurons also evoked brain-wide bloodoxygenation-level-dependent activation, although with a distinct spatiotemporal profile. Our results directly demonstrate that lowfrequency activity governs large-scale, brain-wide connectivity and interactions through long-range excitatory projections to coordinate the functional integration of remote brain regions. This low-frequency phenomenon contributes to the neural basis of long-range functional connectivity as measured by resting-state fMRI.fMRI | optogenetic | brain connectivity | low frequency | thalamus T he brain is a highly complex, interconnected structure with parallel and hierarchical networks distributed within and between neural systems (1, 2). This integrative architecture dictates the underlying principles of how brain-wide neural connectivity supports and organizes sensory, behavioral, and cognitive processes (3). Recent advances in structural (2, 4) and functional connectivity (5-12) mapping, as well as neural circuit modulatory tools, such as optogenetics (13, 14), permit detailed, high-resolution neural examinations at unprecedented scales. In particular, functional connectivity mapping using resting-state functional MRI (rsfMRI) produces noninvasive visualization of slow and spontaneous hemodynamic fluctuations in humans (5-9) and animals (10-12). Coherent low-frequency (<1 Hz) fluctuations across functionally coupled, large-scale networks is an intriguing property, although the exact underlying neural bases and functional significance remain unclear. Previous studies integrating large-scale electrical recordings, voltage-sensitive dye (VSD), and Ca 2+ -imaging techniques (15-18) support the hypothesis that slow, oscillating neural activity constrains and elicits these hemodynamic fluctuations. Furthermore, low-frequency activity can temporally synchronize remote brain region...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Leong

Chan

Gao

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Patterned discharge, such as burst firing and/or oscillatory activity, is particularly relevant for neural processing: bursts often represent units of information (Izhikevich et al, 2003), whereas oscillations provide precise temporal windows of excitability for circuit computations (Mizuseki et al, 2009). Different frequencies have been reported to encode specific brain states (Buzsáki et al, 2013). At the lower end of the time scale, oscillations extend into the slow (0.1-1 Hz) and infraslow (Ͻ0.1 Hz) range (Schroeder and Lakatos, 2009).…”

Section: Introductionmentioning

confidence: 99%

Interdependent Conductances Drive Infraslow Intrinsic Rhythmogenesis in a Subset of Accessory Olfactory Bulb Projection Neurons

Gorin¹,

Tsitoura²,

Kahan

et al. 2016

J. Neurosci.

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The accessory olfactory system controls social and sexual behavior. However, key aspects of sensory signaling along the accessory olfactory pathway remain largely unknown. Here, we investigate patterns of spontaneous neuronal activity in mouse accessory olfactory bulb mitral cells, the direct neural link between vomeronasal sensory input and limbic output. Both in vitro and in vivo, we identify a subpopulation of mitral cells that exhibit slow stereotypical rhythmic discharge. In intrinsically rhythmogenic neurons, these periodic activity patterns are maintained in absence of fast synaptic drive. The physiological mechanism underlying mitral cell autorhythmicity involves cyclic activation of three interdependent ionic conductances: subthreshold persistent Na ϩ current, R-type Ca 2ϩ current, and Ca 2ϩ -activated big conductance K ϩ current. Together, the interplay of these distinct conductances triggers infraslow intrinsic oscillations with remarkable periodicity, a default output state likely to affect sensory processing in limbic circuits.

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“…beta rhythm | magnetoencephalography | computational modeling | sensorimotor processing | Parkinson's disease B eta band rhythms (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29) are a commonly observed activity pattern in the brain. They are found with magnetoencephalography (MEG) (1)(2)(3)(4), EEG (5,6), and local field potential (LFP) recordings from neocortex (7)(8)(9) and are preserved across species (10). Local beta oscillations and their coordination between regions are implicated in numerous functions, including sensory perception, selective attention, and motor planning and initiation (2,3,6,7,9,(11)(12)(13)(14)(15).…”

mentioning

confidence: 99%

Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice

Sherman

Lee

Law

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

417

510

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Human neocortical 15-29-Hz beta oscillations are strong predictors of perceptual and motor performance. However, the mechanistic origin of beta in vivo is unknown, hindering understanding of its functional role. Combining human magnetoencephalography (MEG), computational modeling, and laminar recordings in animals, we present a new theory that accounts for the origin of spontaneous neocortical beta. In our MEG data, spontaneous beta activity from somatosensory and frontal cortex emerged as noncontinuous beta events typically lasting <150 ms with a stereotypical waveform. Computational modeling uniquely designed to infer the electrical currents underlying these signals showed that beta events could emerge from the integration of nearly synchronous bursts of excitatory synaptic drive targeting proximal and distal dendrites of pyramidal neurons, where the defining feature of a beta event was a strong distal drive that lasted one beta period (∼50 ms). This beta mechanism rigorously accounted for the beta event profiles; several other mechanisms did not. The spatial location of synaptic drive in the model to supragranular and infragranular layers was critical to the emergence of beta events and led to the prediction that beta events should be associated with a specific laminar current profile. Laminar recordings in somatosensory neocortex from anesthetized mice and awake monkeys supported these predictions, suggesting this beta mechanism is conserved across species and recording modalities. These findings make several predictions about optimal states for perceptual and motor performance and guide causal interventions to modulate beta for optimal function. beta rhythm | magnetoencephalography | computational modeling | sensorimotor processing | Parkinson's disease B eta band rhythms (15-29 Hz) are a commonly observed activity pattern in the brain. They are found with magnetoencephalography (MEG) (1-4), EEG (5, 6), and local field potential (LFP) recordings from neocortex (7-9) and are preserved across species (10). Local beta oscillations and their coordination between regions are implicated in numerous functions, including sensory perception, selective attention, and motor planning and initiation (2,3,6,7,9,(11)(12)(13)(14)(15). Neocortical beta oscillations are disrupted in various neuropathologies, most notably Parkinson's disease (PD), in which treatments that alleviate motor symptoms also reverse the neocortical beta disruption (16,17). Although associations between beta and performance suggest a crucial role in brain function, beta rhythmicity might not be important per se but instead may be an epiphenomenal consequence of other important processes. Discovering how beta emerges at the cellular and network levels is crucial to understanding why beta is such a clear predictor of performance in many domains.A major, unresolved point of debate concerns the locus of beta generation. One prominent view is that beta is generated in basal ganglia and thalamic structures and that neocortical beta is an entrained reflecti...

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Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms

Cited by 779 publications

References 154 publications

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Interdependent Conductances Drive Infraslow Intrinsic Rhythmogenesis in a Subset of Accessory Olfactory Bulb Projection Neurons

Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice

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