A Beta Oscillation Network in the Rat Olfactory System During a 2-Alternative Choice Odor Discrimination Task

We previously showed that in a two-alternative choice (2AC) task, olfactory bulb (OB) gamma oscillations (∼70 Hz in rats) were enhanced during discrimination of structurally similar odorants (fine discrimination) versus discrimination of dissimilar odorants (coarse discrimination). In other studies (mostly employing go/no-go tasks) in multiple labs, beta oscillations (15–35 Hz) dominate the local field potential (LFP) signal in olfactory areas during odor sampling. Here we analyzed the beta frequency band power and pairwise coherence in the 2AC task. We show that in a task dominated by gamma in the OB, beta oscillations are also present in three interconnected olfactory areas (OB and anterior and posterior pyriform cortex). Only the beta band showed consistently elevated coherence during odor sniffing across all odor pairs, classes (alcohols and ketones), and discrimination types (fine and coarse), with stronger effects in first than in final criterion sessions (>70% correct). In the first sessions for fine discrimination odor pairs, beta power for incorrect trials was the same as that for correct trials for the other odor in the pair. This pattern was not repeated in coarse discrimination, in which beta power was elevated for correct relative to incorrect trials. This difference between fine and coarse odor discriminations may relate to different behavioral strategies for learning to differentiate similar versus dissimilar odors. Phase analysis showed that the OB led both pyriform areas in the beta frequency band during odor sniffing. We conclude that the beta band may be the means by which information is transmitted from the OB to higher order areas, even though task specifics modify dominance of one frequency band over another within the OB.

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Directional Coupling From the Olfactory Bulb to the Hippocampus During a Go/No-Go Odor Discrimination Task

Journal of Neurophysiology ◽

10.1152/jn.01075.2009 ◽

2010 ◽

Vol 103 (5) ◽

pp. 2633-2641 ◽

Cited By ~ 31

Author(s):

Boris Gourévitch ◽

Leslie M. Kay ◽

Claire Martin

Keyword(s):

Olfactory Bulb ◽

Cognitive Processing ◽

Information Transfer ◽

Field Potential ◽

Ventral Hippocampus ◽

Beta Oscillations ◽

Odor Processing ◽

Odor Discrimination Task ◽

Beta Frequency Band ◽

Beta Frequency

The hippocampus and olfactory regions are anatomically close, and both play a major role in memory formation. However, the way they interact during odor processing is still unclear. In both areas, strong oscillations of the local field potential (LFP) can be recorded, and are modulated by behavior. In particular, in the olfactory system, the beta rhythm (15–35 Hz) is associated with cognitive processing of an olfactory stimulus. Using LFP recordings in the olfactory bulb and dorsal and ventral hippocampus during performance of an olfactory go/no-go task in rats, we previously showed that beta oscillations are also present in the hippocampus, coherent with those in the olfactory bulb, during odor sampling. In this study, we provide further insight into information transfer in the olfacto-hippocampal network by using directional coherence (DCOH estimate), a method based on the temporal relation between two or more signals in the frequency domain. In the theta band (6–12 Hz), coherence between the olfactory bulb (OB) and the hippocampus (HPC) is weak and can be both in the feedback and feedforward directions. However, at this frequency, modulation of the coupling between the dorsal and ventral hippocampus is seen during stimulus expectation versus odor processing. In the beta frequency band (15–35 Hz), analysis showed a strong unidirectional coupling from the OB to dorsal and ventral HPC, indicating that, during odor processing, beta oscillations in the hippocampus are driven by the olfactory bulb.

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Granule cell excitability regulates gamma and beta oscillations in a model of the olfactory bulb dendrodendritic microcircuit

Journal of Neurophysiology ◽

10.1152/jn.00988.2015 ◽

2016 ◽

Vol 116 (2) ◽

pp. 522-539 ◽

Cited By ~ 24

Author(s):

Bolesław L. Osinski ◽

Leslie M. Kay

Keyword(s):

Olfactory Bulb ◽

Granule Cells ◽

Field Potential ◽

Gamma Oscillations ◽

Causal Link ◽

Beta Oscillations ◽

Gamma Frequency ◽

Voltage Dependent ◽

Nmda Channels ◽

Beta Frequency

Odors evoke gamma (40–100 Hz) and beta (20–30 Hz) oscillations in the local field potential (LFP) of the mammalian olfactory bulb (OB). Gamma (and possibly beta) oscillations arise from interactions in the dendrodendritic microcircuit between excitatory mitral cells (MCs) and inhibitory granule cells (GCs). When cortical descending inputs to the OB are blocked, beta oscillations are extinguished whereas gamma oscillations become larger. Much of this centrifugal input targets inhibitory interneurons in the GC layer and regulates the excitability of GCs, which suggests a causal link between the emergence of beta oscillations and GC excitability. We investigate the effect that GC excitability has on network oscillations in a computational model of the MC-GC dendrodendritic network with Ca2+-dependent graded inhibition. Results from our model suggest that when GC excitability is low, the graded inhibitory current mediated by NMDA channels and voltage-dependent Ca2+ channels (VDCCs) is also low, allowing MC populations to fire in the gamma frequency range. When GC excitability is increased, the activation of NMDA receptors and other VDCCs is also increased, allowing the slow decay time constants of these channels to sustain beta-frequency oscillations. Our model argues that Ca2+ flow through VDCCs alone could sustain beta oscillations and that the switch between gamma and beta oscillations can be triggered by an increase in the excitability state of a subpopulation of GCs.

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Surprise About Sensory Event Timing Drives Cortical Transients in the Beta Frequency Band

10.1101/254060 ◽

2018 ◽

Author(s):

T. Meindertsma ◽

N.A. Kloosterman ◽

A.K. Engel ◽

E.J. Wagenmakers ◽

T.H. Donner

Keyword(s):

Frequency Band ◽

Ideal Observer ◽

Beta Band ◽

Statistical Structure ◽

Population Activity ◽

Sensory Event ◽

Event Timing ◽

Beta Frequency Band ◽

Observer Model ◽

Beta Frequency

AbstractLearning the statistical structure of the environment is crucial for adaptive behavior. Humans and non-human decision-makers seem to track such structure through a process of probabilistic inference, which enables predictions about behaviorally relevant events. Deviations from such predictions cause surprise, which in turn helps improve inference. Surprise about the timing of behaviorally relevant sensory events drives phasic responses of neuromodulatory brainstem systems, which project to the cerebral cortex. Here, we developed a computational model-based magnetoencephalography (MEG) approach for mapping the resulting cortical transients across space, time, and frequency, in the human brain (N=28, 17 female). We used a Bayesian ideal observer model to learn the statistics of the timing of changes in a simple visual detection task. This model yielded quantitative trial-by-trial estimates of temporal surprise. The model-based surprise variable predicted trial-by trial variations in reaction time more strongly than the externally observable interval timings alone. Trial-by-trial variations in surprise were negatively correlated with the power of cortical population activity measured with MEG. This surprise-related power suppression occurred transiently around the behavioral response, specifically in the beta frequency band. It peaked in parietal and prefrontal cortices, remote from the motor cortical suppression of beta power related to overt report (button press) of change detection. Our results indicate that surprise about sensory event timing transiently suppresses ongoing beta-band oscillations in association cortex. This transient suppression of frontal beta-band oscillations might reflect an active reset triggered by surprise, and is in line with the idea that beta-oscillations help maintain cognitive sets.Significance statementThe brain continuously tracks the statistical structure of the environment to anticipate behaviorally relevant events. Deviations from such predictions cause surprise, which in turn drives neural activity in subcortical brain regions that project to the cerebral cortex. We used magnetoencephalography in humans to map out surprise-related modulations of cortical population activity across space, time, and frequency. Surprise was elicited by variable timing of visual stimulus changes requiring a behavioral response. Surprise was quantified by means of an ideal observer model. Surprise predicted behavior as well as a transient suppression of beta frequency band oscillations in frontal cortical regions. Our results are in line with conceptual accounts that have linked neural oscillations in the beta-band to the maintenance of cognitive sets.

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Pharmacological manipulation of the olfactory bulb modulates beta oscillations: testing model predictions

Journal of Neurophysiology ◽

10.1152/jn.00090.2018 ◽

2018 ◽

Vol 120 (3) ◽

pp. 1090-1106 ◽

Cited By ~ 7

Author(s):

Bolesław L. Osinski ◽

Alex Kim ◽

Wenxi Xiao ◽

Nisarg M. Mehta ◽

Leslie M. Kay

Keyword(s):

Nmda Receptor ◽

Olfactory Bulb ◽

Local Field ◽

Local Field Potential ◽

Field Potential ◽

Gamma Oscillations ◽

Receptor Activation ◽

Beta Oscillations ◽

Pyriform Cortex ◽

Beta Power

The mammalian olfactory bulb (OB) generates gamma (40–100 Hz) and beta (15–30 Hz) local field potential (LFP) oscillations. Gamma oscillations arise at the peak of inhalation supported by dendrodendritic interactions between glutamatergic mitral cells (MCs) and GABAergic granule cells (GCs). Beta oscillations are induced by odorants in learning or odor sensitization paradigms, but their mechanism and function are still poorly understood. When centrifugal OB inputs are blocked, beta oscillations disappear, but gamma oscillations persist. Centrifugal inputs target primarily GABAergic interneurons in the GC layer (GCL) and regulate GC excitability, suggesting a causal link between beta oscillations and GC excitability. Our previous modeling work predicted that convergence of excitatory/inhibitory inputs onto MCs and centrifugal inputs onto GCs increase GC excitability sufficiently to produce beta oscillations primarily through voltage dependent calcium channel-mediated GABA release, independently of NMDA channels. We test some of the predictions of this model by examining the influence of NMDA and muscarinic acetylcholine (ACh) receptors, which affect GC excitability in different ways, on beta oscillations. A few minutes after intrabulbar infusion, scopolamine (muscarinic antagonist) suppressed odor-evoked beta in response to a strong stimulus but increased beta power in response to a weak stimulus, as predicted by our model. Pyriform cortex (PC) beta power was unchanged. Oxotremorine (muscarinic agonist) suppressed all oscillations, likely from overinhibition. APV, an NMDA receptor antagonist, suppressed gamma oscillations selectively (in OB and PC), lending support to the model’s prediction that beta oscillations can be supported independently of NMDA receptors. NEW & NOTEWORTHY Olfactory bulb local field potential beta oscillations appear to be gated by GABAergic granule cell excitability. Reducing excitability with scopolamine reduces beta induced by strong odors but increases beta induced by weak odors. Beta oscillations rely on the same synapse as gamma oscillations but, unlike gamma, can persist in the absence of NMDA receptor activation. Pyriform cortex beta oscillations maintain power when olfactory bulb beta power is low, and the system maintains beta band coherence.

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Phase-specific microstimulation in brain machine interface setting differentially modulates beta oscillations and affects behavior

10.1101/622787 ◽

2019 ◽

Cited By ~ 2

Author(s):

Oren Peles ◽

Uri Werner-Reiss ◽

Hagai Bergman ◽

Zvi Israel ◽

Eilon Vaadia

Keyword(s):

Field Potential ◽

Reaction Times ◽

Brain Diseases ◽

Brain Machine Interface ◽

Success Rates ◽

Beta Band ◽

Beta Oscillations ◽

Local Networks ◽

Beta Power ◽

Machine Interface

SummaryIt is widely accepted that beta-band oscillations play a role in sensorimotor behavior. To further explore this role, we developed a novel hybrid platform to combine operant conditioning and phase-specific intracortical microstimulation (ICMS). We trained monkeys, implanted with 96 electrodes arrays in motor cortex, to volitionally enhance local field potential (LFP) beta-band (20-30Hz) activity at selected sites using a brain-machine interface (BMI). We demonstrate that beta oscillations of LFP and single-unit spiking activity increased dramatically with BMI training, and that pre-movement Beta-power was anti-correlated with task performance. We also show that phase-specific ICMS modulated the power and phase of oscillations, shifting local networks between oscillatory and non-oscillatory states. Furthermore, ICMS induced phase-dependent effects in animal reaction times and success rates. These findings contribute to unraveling of the functional role of cortical oscillations, and to future development of clinical tools for ameliorating abnormal neuronal activities in brain diseases.

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Pharmacological manipulation of olfactory bulb granule cell excitability modulates beta oscillations: Testing a model

10.1101/234625 ◽

2017 ◽

Author(s):

Boleslaw L. Osinski ◽

Alex Kim ◽

Wenxi Xiao ◽

Nisarg Mehta ◽

Leslie M. Kay

Keyword(s):

Olfactory Bulb ◽

Granule Cell ◽

Piriform Cortex ◽

Field Potential ◽

Gamma Oscillations ◽

List Type ◽

Muscarinic Agonist ◽

Beta Oscillations ◽

Cell Excitability ◽

Beta Power

AbstractThe mammalian olfactory bulb (OB) generates gamma (40 – 100 Hz) and beta (15 – 30 Hz) oscillations of the local field potential (LFP). Gamma oscillations arise at the peak of inhalation supported by dendrodendritic interactions between glutamatergic mitral cells (MCs) and GABAergic granule cells (GCs). Beta oscillations occur in response to odorants in learning or odor sensitization paradigms, but their generation mechanism and function are still poorly understood. When centrifugal inputs to the OB are blocked, beta oscillations disappear, but gamma oscillations persist. Centrifugal input targets primarily GABAergic interneurons in the GC layer (GCL) and regulates GC excitability, which suggests a causal link between beta oscillations and GC excitability. Previous modeling work from our laboratory predicted that convergence of excitatory/inhibitory inputs onto MCs and centrifugal inputs onto GCs can increase GC excitability sufficiently to drive beta oscillations primarily through voltage dependent calcium channel (VDCC) mediated GABA release, independently of NMDA channels. We test this model by examining the influence of NMDA and muscarinic acetylcholine receptors on GC excitability and beta oscillations. Intrabulbar scopolamine (muscarinic antagonist) infusion decreased or completely suppressed odor-evoked beta in response to a strong stimulus, but increased beta power in response to a weak stimulus, as predicted by our model. Piriform cortex (PC) beta power was unchanged. Oxotremorine (muscarinic agonist) tended to suppress all oscillations, probably from over-inhibition. APV, an NMDA receptor antagonist, suppressed gamma oscillations selectively (in OB and PC), lending support to the model’s prediction that beta oscillations can be supported by VDCC mediated currents.New and Noteworthy:Olfactory bulb beta oscillations rely on granule cell excitability.Reducing granule cell excitability with scopolamine reduces high volatilityinduced beta power but increases low volatility-induced beta power.Piriform cortex beta oscillations maintain power when olfactory bulb beta power is low, and the system maintains beta band coherence.

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Beta-frequency electrophysiological bursts: BOLD correlates and relationships with psychotic illness

BJPsych Open ◽

10.1192/bjo.2021.151 ◽

2021 ◽

Vol 7 (S1) ◽

pp. S37-S38

Author(s):

Paul M Briley ◽

Elizabeth B Liddle ◽

Karen J Mullinger ◽

Molly Simmonite ◽

Lena Palaniyappan ◽

...

Keyword(s):

Working Memory ◽

Frequency Band ◽

Blood Oxygenation ◽

Healthy Controls ◽

Psychotic Illness ◽

Beta Power ◽

Eeg Data ◽

Beta Frequency Band ◽

Sensorimotor Information ◽

Beta Frequency

AimsTo identify the BOLD (blood oxygenation level dependent) correlates of bursts of beta frequency band electrophysiological activity, and to compare BOLD responses between healthy controls and patients with psychotic illness.The post movement beta rebound (PMBR) is a transient increase in power in the beta frequency band (13-30 Hz), recorded with methods such as electroencephalography (EEG), following the completion of a movement. PMBR size is reduced in patients with schizophrenia and inversely correlated with severity of illness. PMBR size is inversely correlated with measures of schizotypy in non-clinical groups. Therefore, beta-band activity may reflect a fundamental neural process whose disruption plays an important role in the pathophysiology of schizophrenia. Recent work has found that changes in beta power reflect changes in the probability-of-occurrence of transient bursts of beta-frequency activity. Understanding the generators of beta bursts could help unravel the pathophysiology of psychotic illness and thus identify novel treatment targets.MethodEEG data were recorded simultaneously with BOLD data measured with 3T functional magnetic resonance imaging (fMRI), whilst participants performed an n-back working memory task. We included seventy-eight participants – 32 patients with schizophrenia, 16 with bipolar disorder and 30 healthy controls. Beta bursts were identified in the EEG data using a thresholding method and burst timings were used as markers in an event-related fMRI design convolved with a conventional haemodynamic response function. A region of interest analysis compared beta-event-related BOLD activity between patients and controls.ResultBeta bursts phasically activated brain regions implicated in coding task-relevant content (specifically, regions involved in the phonological representation of letter stimuli, as well as areas representing motor responses). Further, bursts were associated with suppression of tonically-active regions. In the EEG, PMBR was greater in controls than patients, and, in patients, PMBR size was positively correlated with Global Assessment of Functioning scores, and negatively correlated with persisting symptoms of disorganisation and performance on a digit symbol substition test. Despite this, patients showed greater, more extensive, burst-related BOLD activation than controls.ConclusionOur findings are consistent with a recent model in which beta bursts serve to reactivate latently-maintained, task-relevant, sensorimotor information. The increased BOLD response associated with bursts in patients, despite reduced PMBR, could reflect inefficiency of burst-mediated cortical synchrony, or it may suggest that the sensorimotor information reactivated by beta bursts is less precisely specified in psychosis. We propose that dysfunction of the mechanisms by which beta bursts reactivate task-relevant content can manifest as disorganisation and working memory deficits, and may contribute to persisting symptoms and impairment in psychosis.

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