scholarly journals Learning improves decoding of odor identity with phase-referenced oscillations in the olfactory bulb

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Justin Losacco ◽  
Daniel Ramirez-Gordillo ◽  
Jesse Gilmer ◽  
Diego Restrepo
Keyword(s):  
Olfactory Bulb ◽  
Field Potential ◽  
Brain Regions ◽  
Spike Timing ◽  
Potential Oscillations ◽  
Neuronal Ensembles ◽  
Beta Power ◽  
High Gamma ◽  
Theta Phase ◽  
Phase Amplitude

Local field potential oscillations reflect temporally coordinated neuronal ensembles—coupling distant brain regions, gating processing windows, and providing a reference for spike timing-based codes. In phase amplitude coupling (PAC), the amplitude of the envelope of a faster oscillation is larger within a phase window of a slower carrier wave. Here, we characterized PAC, and the related theta phase-referenced high gamma and beta power (PRP), in the olfactory bulb of mice learning to discriminate odorants. PAC changes throughout learning, and odorant-elicited changes in PRP increase for rewarded and decrease for unrewarded odorants. Contextual odorant identity (is the odorant rewarded?) can be decoded from peak PRP in animals proficient in odorant discrimination, but not in naïve mice. As the animal learns to discriminate the odorants the dimensionality of PRP decreases. Therefore, modulation of phase-referenced chunking of information in the course of learning plays a role in early sensory processing in olfaction.

scholarly journals Learning improves decoding of odor identity with phase-referenced oscillations in the olfactory bulb

2019 ◽  
Author(s):  
Justin Losacco ◽  
Daniel Ramirez-Gordillo ◽  
Jesse Gilmer ◽  
Diego Restrepo
Keyword(s):  
Olfactory Bulb ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Brain Regions ◽  
Spike Timing ◽  
Potential Oscillations ◽  
Theta Oscillation ◽  
Beta Power ◽  
Early Processing ◽  
Theta Phase

AbstractLocal field potential oscillations reflect temporally coordinated neuronal ensembles— coupling distant brain regions, gating processing windows, and providing a reference for spike timing-based codes. In phase amplitude coupling (PAC), the amplitude of the envelope of a faster oscillation is larger within a phase window of a slower carrier wave. Here, we characterized PAC, and the related theta phase-referenced high gamma and beta power (PRP), in the olfactory bulb of mice learning to discriminate odorants. PAC changes throughout learning, and odorant-elicited changes in PRP increase for rewarded and decrease for unrewarded odorants. Contextual odorant identity (is the odorant rewarded?) can be decoded from peak PRP in animals proficient in odorant discrimination, but not in naïve mice. As the animal learns to discriminate the odorants the dimensionality of PRP decreases. Therefore, modulation of phase-referenced chunking of information in the course of learning plays a role in early sensory processing in olfaction.SignificanceEarly processing of olfactory information takes place in circuits undergoing slow frequency theta oscillations generated by the interplay of olfactory input modulated by sniffing and centrifugal feedback from downstream brain areas. Studies in the hippocampus and cortex suggest that different information “chunks” are conveyed at different phases of the theta oscillation. Here we show that in the olfactory bulb, the first processing station in the olfactory system, the amplitude of high frequency gamma oscillations encodes for information on whether an odorant is rewarded when it is observed at the peak phase of the theta oscillation. Furthermore, encoding of information by the theta phase-referenced gamma oscillations becomes more accurate as the animal learns to differentiate two odorants.

scholarly journals Transformation of Independent Oscillatory Inputs into Temporally Precise Rate Codes

2016 ◽  
Author(s):  
David Tingley ◽  
Andrew A. Alexander ◽  
Laleh K. Quinn ◽  
Andrea A. Chiba ◽  
Douglas Nitz
Keyword(s):  
Field Potential ◽  
Spatial Location ◽  
Brain Regions ◽  
Synaptic Activity ◽  
Specific Rate ◽  
Attention Task ◽  
Potential Oscillations ◽  
Phase Precession ◽  
Theta Phase ◽  
Theta Phase Precession

AbstractComplex behaviors demand temporal coordination among functionally distinct brain regions. The basal forebrain’s afferent and efferent structure suggests a capacity for mediating such coordination. During performance of a selective attention task, synaptic activity in this region was dominated by four amplitude-independent oscillations temporally organized by the phase of the slowest, a theta rhythm. Further, oscillatory amplitudes were precisely organized by task epoch and a robust input/output transform, from synchronous synaptic activity to spiking rates of basal forebrain neurons, was identified. For many neurons, spiking was temporally organized as phase precessing sequences against theta band field potential oscillations. Remarkably, theta phase precession advanced in parallel to task progression, rather than absolute spatial location or time. Together, the findings reveal a process by which associative brain regions can integrate independent oscillatory inputs and transform them into sequence-specific, rate-coded outputs that are adaptive to the pace with which organisms interact with their environment.

scholarly journals Interactions between motor thalamic field potentials and single unit spiking predict behavior in rats

2019 ◽  
Author(s):  
Matt Gaidica ◽  
Amy Hurst ◽  
Christopher Cyr ◽  
Daniel K. Leventhal
Keyword(s):  
Task Performance ◽  
Brain Activity ◽  
Field Potential ◽  
Spike Timing ◽  
Delta Phase ◽  
Beta Power ◽  
High Gamma ◽  
Gamma Power ◽  
Complex Relationships ◽  
And Behavior

AbstractThe thalamus plays a central role in generating circuit-level neural oscillations believed to coordinate brain activity over large spatiotemporal scales. Such thalamic influences are well-documented for sleep rhythms and in sensory systems, but the relationship between thalamic activity, motor circuit local field potential (LFP) oscillations, and behavior is unknown. We recorded wideband motor thalamic (Mthal) electrophysiology as healthy rats performed a two-alternative forced choice task. The power of delta (1−4 Hz), beta (13−30 Hz), low gamma (30−70 Hz), and high gamma (70−200 Hz) oscillations were strongly modulated by task performance. As in cortex, delta phase predicted beta/low gamma power and reaction time. Furthermore, delta phase differentially predicted spike timing in functionally distinct populations of Mthal neurons, which also predicted task performance and beta power. These complex relationships suggest mechanisms for commonly observed LFP-LFP and spike-LFP interactions, as well as subcortical influences on motor output.

scholarly journals Induced cortical oscillations in turtle cortex are coherent at the mesoscale of population activity, but not at the microscale of the membrane potential of neurons

2017 ◽  
Vol 118 (5) ◽  
pp. 2579-2591 ◽  
Author(s):  
Mahmood S. Hoseini ◽  
Jeff Pobst ◽  
Nathaniel Wright ◽  
Wesley Clawson ◽  
Woodrow Shew ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Membrane Potential ◽  
Neural Activity ◽  
Visual Stimulation ◽  
Field Potential ◽  
Brain Regions ◽  
Large Trial ◽  
Population Activity ◽  
Potential Oscillations ◽  
Time Frequency

Bursts of oscillatory neural activity have been hypothesized to be a core mechanism by which remote brain regions can communicate. Such a hypothesis raises the question to what extent oscillations are coherent across spatially distant neural populations. To address this question, we obtained local field potential (LFP) and membrane potential recordings from the visual cortex of turtle in response to visual stimulation of the retina. The time-frequency analysis of these recordings revealed pronounced bursts of oscillatory neural activity and a large trial-to-trial variability in the spectral and temporal properties of the observed oscillations. First, local bursts of oscillations varied from trial to trial in both burst duration and peak frequency. Second, oscillations of a given recording site were not autocoherent; i.e., the phase did not progress linearly in time. Third, LFP oscillations at spatially separate locations within the visual cortex were more phase coherent in the presence of visual stimulation than during ongoing activity. In contrast, the membrane potential oscillations from pairs of simultaneously recorded pyramidal neurons showed smaller phase coherence, which did not change when switching from black screen to visual stimulation. In conclusion, neuronal oscillations at distant locations in visual cortex are coherent at the mesoscale of population activity, but coherence is largely absent at the microscale of the membrane potential of neurons. NEW & NOTEWORTHY Coherent oscillatory neural activity has long been hypothesized as a potential mechanism for communication across locations in the brain. In this study we confirm the existence of coherent oscillations at the mesoscale of integrated cortical population activity. However, at the microscopic level of neurons, we find no evidence for coherence among oscillatory membrane potential fluctuations. These results raise questions about the applicability of the communication through coherence hypothesis to the level of the membrane potential.

Phasic Stimuli Evoke Precisely Timed Spikes in Intermittently Discharging Mitral Cells

2004 ◽  
Vol 92 (2) ◽  
pp. 743-753 ◽  
Author(s):  
Ramani Balu ◽  
Phillip Larimer ◽  
Ben W. Strowbridge
Keyword(s):  
Olfactory Bulb ◽  
Action Potentials ◽  
Sensory Stimulation ◽  
Spike Timing ◽  
Mitral Cells ◽  
Potential Oscillations ◽  
Sensory Stimuli ◽  
Subthreshold Oscillations ◽  
Simple Step

Mitral cells, the principal cells of the olfactory bulb, respond to sensory stimulation with precisely timed patterns of action potentials. By contrast, the same neurons generate intermittent spike clusters with variable timing in response to simple step depolarizations. We made whole cell recordings from mitral cells in rat olfactory bulb slices to examine the mechanisms by which normal sensory stimuli could generate precisely timed spike clusters. We found that individual mitral cells fired clusters of action potentials at 20-40 Hz, interspersed with periods of subthreshold membrane potential oscillations in response to depolarizing current steps. TTX (1 μM) blocked a sustained depolarizing current and fast subthreshold oscillations in mitral cells. Phasic stimuli that mimic trains of slow excitatory postsynaptic potentials (EPSPs) that occur during sniffing evoked precisely timed spike clusters in repeated trials. The amplitude of the first simulated EPSP in a train gated the generation of spikes on subsequent EPSPs. 4-aminopyridine (4-AP)–sensitive K+ channels are critical to the generation of spike clusters and reproducible spike timing in response to phasic stimuli. Based on these results, we propose that spike clustering is a process that depends on the interaction between a 4-AP–sensitive K+ current and a subthreshold TTX-sensitive Na+ current; interactions between these currents may allow mitral cells to respond selectively to stimuli in the theta frequency range. These intrinsic properties of mitral cells may be important for precisely timing spikes evoked by phasic stimuli that occur in response to odor presentation in vivo.

scholarly journals The Olfactory Bulb Facilitates Use of Category Bounds for Classification of Odorants in Different Intensity Groups

2020 ◽  
Vol 14 ◽  
Author(s):  
Justin Losacco ◽  
Nicholas M. George ◽  
Naoki Hiratani ◽  
Diego Restrepo
Keyword(s):  
Decision Making ◽  
Olfactory Bulb ◽  
Field Potential ◽  
Odor Concentration ◽  
Linear Discriminant ◽  
Percent Correct ◽  
Theta Phase ◽  
Decoding Accuracy ◽  
Local Field Potential Lfp

Signal processing of odor inputs to the olfactory bulb (OB) changes through top-down modulation whose shaping of neural rhythms in response to changes in stimulus intensity is not understood. Here we asked whether the representation of a high vs. low intensity odorant in the OB by oscillatory neural activity changed as the animal learned to discriminate odorant concentration ranges in a go-no go task. We trained mice to discriminate between high vs. low concentration odorants by learning to lick to the rewarded group (low or high). We recorded the local field potential (LFP) in the OB of these mice and calculated the theta-referenced beta or gamma oscillation power (theta phase-referenced power, or tPRP). We found that as the mouse learned to differentiate odorant concentrations, tPRP diverged between trials for the rewarded vs. the unrewarded concentration range. For the proficient animal, linear discriminant analysis was able to predict the rewarded odorant group and the performance of this classifier correlated with the percent correct behavior in the odor concentration discrimination task. Interestingly, the behavioral response and decoding accuracy were asymmetric as a function of concentration when the rewarded stimulus was shifted between the high and low odorant concentration ranges. A model for decision making motivated by the statistics of OB activity that uses a single threshold in a logarithmic concentration scale displays this asymmetry. Taken together with previous studies on the intensity criteria for decisions on odorant concentrations, our finding suggests that OB oscillatory events facilitate decision making to classify concentrations using a single intensity criterion.

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

2018 ◽  
Vol 120 (3) ◽  
pp. 1090-1106 ◽  
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.

scholarly journals How Global Are Olfactory Bulb Oscillations?

2010 ◽  
Vol 104 (3) ◽  
pp. 1768-1773 ◽  
Author(s):  
Leslie M. Kay ◽  
Philip Lazzara
Keyword(s):  
Olfactory Bulb ◽  
Local Field ◽  
Local Field Potential ◽  
Field Potential ◽  
Beta Band ◽  
Recording Site ◽  
Potential Oscillations ◽  
Frequency Bands ◽  
Surface Electrodes ◽  
Analysis Window

Previous studies in waking animals have shown that the frequency structure of olfactory bulb (OB) local field potential oscillations is very similar across the OB, but large low-impedance surface electrodes may have favored highly coherent events, averaging out local inhomogeneities. We tested the hypothesis that OB oscillations represent spatially homogeneous phenomena at all scales. We used pairs of concentric electrodes (200 μm outer shaft surrounding an inner 2–3 μm recording site) beginning on the dorsal OB at anterior and medial locations in urethane-anesthetized rats and measured local field potential responses at successive 200 μm depths before and during odor stimulation. Within locations (outer vs. inner lead on a single probe), on the time scale of 0.5 s, coherence in all frequency bands was significant, but on larger time scales (10 s), only respiratory (1–4 Hz) and beta (15–30 Hz) oscillations showed prominent peaks. Across locations, coherence in all frequency bands was significantly lower for both sizes of electrodes at all depths but the most superficial 600 μm. Near the pial surface, coherence across outer (larger) electrodes at different sites was equal to coherence across outer and inner (small) electrodes within a single site and larger than coherence across inner electrodes at different sites. Overall, the beta band showed the largest coherence across bulbar sites and electrodes. Therefore larger electrodes at the surface of the OB favor globally coherent events, and at all depths, coherence depends on the type of oscillation (beta or gamma) and duration of the analysis window.

scholarly journals Nonsinusoidal oscillations underlie pathological phase-amplitude coupling in the motor cortex in Parkinson’s disease

2016 ◽  
Author(s):  
Scott R. Cole ◽  
Erik J. Peterson ◽  
Roemer van der Meij ◽  
Coralie de Hemptinne ◽  
Philip A. Starr ◽  
...  
Keyword(s):  
Parkinson’S Disease ◽  
Parkinson's Disease ◽  
Basal Ganglia ◽  
Motor Cortex ◽  
Field Potential ◽  
Synaptic Activity ◽  
Motor Deficit ◽  
Beta Oscillations ◽  
High Gamma ◽  
Phase Amplitude

AbstractParkinson’s disease (PD) is associated with abnormal beta oscillations (13-30 Hz) in the basal ganglia and motor cortex (M1). Recent reports show that M1 beta-high gamma (50-200 Hz) phase-amplitude coupling (PAC) is exaggerated in PD and is reduced following acute deep brain stimulation (DBS). Here we analyze invasive M1 electrocorticography recordings in PD patients on and off DBS, and in isolated cervical dystonia patients, and show that M1 beta oscillations are nonsinusoidal, having sharp and asymmetric features. These sharp oscillatory beta features underlie the previously reported PAC, providing an alternative to the standard interpretation of PAC as an interaction between two distinct frequency components. Specifically, the ratio between peak and trough sharpness is nearly perfectly correlated with beta-high gamma PAC (r = 0.96) and predicts PD-related motor deficit. Using a simulation of the local field potential, we demonstrate that sharp oscillatory waves can arise from synchronous synaptic activity. We propose that exaggerated beta-high gamma PAC may actually reflect such synchronous synaptic activity, manifesting as sharp beta oscillations that are “smoothed out” with DBS. These results support the “desynchronization” hypothesis of DBS wherein DBS counteracts pathological synchronization throughout the basal ganglia-thalamocortical loop. We argue that PAC can be influenced by more than one mechanism. In this case synaptic synchrony, rather than the often assumed spike-field coherence, may underlie exaggerated PAC. These often overlooked temporal features of the oscillatory waveform carry critical physiological information about neural processes and dynamics that may lead to better understanding of underlying neuropathology.

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