scholarly journals Gamma oscillations in the rat ventral striatum originate in the piriform cortex

2017 ◽  
Author(s):  
James E. Carmichael ◽  
Jimmie M. Gmaz ◽  
Matthijs A. A. van der Meer

AbstractLocal field potentials (LFP) recorded from the human and rodent ventral striatum (vStr) exhibit prominent, behaviorally relevant gamma-band oscillations. These oscillations are related to local spiking activity and transiently synchronize with anatomically related areas, suggesting a possible role in organizing vStr activity. However, the origin of vStr gamma is unknown. We recorded vStr gamma oscillations across a 1.4mm2 grid spanned by 64 recording electrodes as rats rested and foraged for rewards, revealing a highly consistent power gradient originating in the adjacent piriform cortex. Phase differences across the vStr were consistently small (<10°) and current source density analysis further confirmed the absence of local sink-source pairs in the vStr. Reversible occlusions of the ipsilateral (but not contralateral) nostril, known to abolish gamma oscillations in the piriform cortex, strongly reduced vStr gamma power and the occurrence of transient gamma-band events. These results imply that local circuitry is not a major contributor to gamma oscillations in the vStr LFP, and that piriform cortex is an important driver of gamma-band oscillations in the vStr and associated limbic areas.Significance StatementThe ventral striatum is an area of anatomical convergence in circuits underlying motivated behavior, but it remains unclear how its inputs from different sources interact. One of the major proposals of how neural circuits may dynamically switch between convergent inputs is through temporal organization reflected in local field potential (LFP) oscillations. Our results show that in the rat, the mechanisms controlling vStr gamma oscillations are primarily located in the in the adjacent piriform cortex, rather than vStr itself. This provides a novel interpretation of previous rodent work on gamma oscillations in the vStr and related circuits, and an important consideration for future work seeking to use oscillations in these areas as biomarkers in rodent models of human behavioral and neurological disorders.


2007 ◽  
Vol 98 (1) ◽  
pp. 394-404 ◽  
Author(s):  
Catherine A. Lowry ◽  
Leslie M. Kay

Recent studies have pointed to olfactory system beta oscillations of the local field potential (15–30 Hz) and their roles both in learning and as specific responses to predator odors. To describe odorant physical properties, resultant behavioral responses and changes in the central olfactory system that may induce these oscillations without associative learning, we tested rats with 26 monomolecular odorants spanning 6 log units of theoretical vapor pressure (estimate of relative vapor phase concentration) and 10 different odor mixtures. We found odorant vapor phase concentration to be inversely correlated with investigation time on the first presentation, after which investigation times were brief and not different across odorants. Analysis of local field potentials from the olfactory bulb and anterior piriform cortex shows that beta oscillations in waking rats occur specifically in response to the class of volatile organic compounds with vapor pressures of 1–120 mmHg. Beta oscillations develop over the first three to four presentations and are weakly present for some odorants in anesthetized rats. Gamma oscillations show a smaller effect that is not restricted to the same range of odorants. Olfactory bulb theta oscillations were also examined as a measure of effective afferent input strength, and the power of these oscillations did not vary systematically with vapor pressure, suggesting that it is not olfactory bulb drive strength that determines the presence of beta oscillations. Theta band coherence analysis shows that coupling strength between the olfactory bulb and piriform cortex increases linearly with vapor phase concentration, which may facilitate beta oscillations above a threshold.



2019 ◽  
Author(s):  
James E. Carmichael ◽  
Matthew M. Yuen ◽  
Matthijs A. A. van der Meer

AbstractOscillations in the local field potential (LFP) are widespread throughout the rodent limbic system, including in structures such as the orbitofrontal cortex and nucleus accumbens. Synchrony between LFPs across these structures, as seen during specific behavioral events, is often interpreted as evidence of a functional interaction. However, the source of these oscillations is often tacitly assumed to be local, leading to a potential misattribution of function. Using in vivo simultaneous multisite recordings in freely moving male rats (n = 7) we demonstrate that gamma-band LFP oscillations (45-90 Hz) in multiple anterior limbic structures are highly synchronous not only with each other, but also with those in piriform cortex. Phase reversals across the piriform cortex cell layer and susceptibility to nasal occlusion indicate that piriform cortex is the source of these common gamma oscillations. Thus, gamma-band LFP oscillations seen in brain regions adjacent to the piriform cortex are likely not generated locally, but are instead volume conducted from the piriform cortex. This emerging view of gamma oscillations in anterior limbic circuits highlights the importance of the common piriform cortex input as a major influence and introduces caveats in the interpretation of locally recorded LFPs.



2018 ◽  
Author(s):  
Hyeyoung Shin ◽  
Christopher I. Moore

Persistent gamma oscillations (30-55Hz) are hypothesized to temporally coordinate stimulus encoding, enabling perception. This prediction poses a conundrum: How can gamma serve as a template when the stimulus itself drives its mediators, presumably perturbing its maintenance? Specifically, fast-spiking interneurons (FS), a key gamma generator, can be highly sensory responsive. Further, the gamma-band local field potential (LFP) shows properties inconsistent with temporal coordination. Combining tetrode recording with controlled psychophysics revealed an FS subtype (γnsFS) that was not sensory responsive, whose inter-spike intervals peaked at gamma, and that fired with higher periodicity than other FS. Successful detection was predicted by increased regularity in γnsFS spiking at gamma, persisting from before to after sensory onset. In contrast, gamma LFP power negatively predicted detection, and was negatively related to gamma band spiking by γnsFS. These results suggest that a distinct interneuron subgroup, not ‘distracted’ by sensory input, mediates perceptually-relevant oscillations independent of LFP.



2010 ◽  
Vol 103 (3) ◽  
pp. 1658-1672 ◽  
Author(s):  
Tobias Kalenscher ◽  
Carien S. Lansink ◽  
Jan V. Lankelma ◽  
Cyriel M. A. Pennartz

Oscillations of local field potentials (LFPs) in the gamma range are found in many brain regions and are supposed to support the temporal organization of cognitive, perceptual, and motor functions. Even though gamma oscillations have also been observed in ventral striatum, one of the brain's most important structures for motivated behavior and reward processing, their specific function during ongoing behavior is unknown. Using a movable tetrode array, we recorded LFPs and activity of neural ensembles in the ventral striatum of rats performing a reward-collection task. Rats were running along a triangle track and in each round collected one of three different types of rewards. The gamma power of LFPs on subsets of tetrodes was modulated by reward-site visits, discriminated between reward types, between baitedness of reward locations and was different before versus after arrival at a reward site. Many single units in ventral striatum phase-locked their discharge pattern to the gamma oscillations of the LFPs. Phase-locking occurred more often in reward-related than in reward-unrelated neurons and LFPs. A substantial number of simultaneously recorded LFPs correlated poorly with each other in terms of gamma rhythmicity, indicating that the expression of gamma activity was heterogeneous and regionally differentiated. The orchestration of LFPs and single-unit activity by way of gamma rhythmicity sheds light on the functional architecture of the ventral striatum and the temporal coordination of ventral striatal activity for modulating downstream areas and regulating synaptic plasticity.



2004 ◽  
Vol 92 (2) ◽  
pp. 1226-1235 ◽  
Author(s):  
Douglas A. Caruana ◽  
C. Andrew Chapman

Although a major output of the hippocampal formation is from the subiculum to the deep layers of the entorhinal cortex, the parasubiculum projects to the superficial layers of the entorhinal cortex and may therefore modulate how the entorhinal cortex responds to sensory inputs from other cortical regions. Recordings at multiple depths in the entorhinal cortex were first used to characterize field potentials evoked by stimulation of the parasubiculum in urethan-anesthetized rats. Current source density analysis showed that a prominent surface-negative field potential component is generated by synaptic activation in layer II. The surface-negative field potential was also observed in rats with chronically implanted electrodes. The response was maintained during short stimulation trains of ≤125 Hz, suggesting that it is generated by activation of monosynaptic inputs to the entorhinal cortex. The piriform cortex also projects to layer II of the entorhinal cortex, and interactions between parasubicular and piriform cortex inputs were investigated using double-site stimulation tests. Simultaneous activation of parasubicular and piriform cortex inputs with high-intensity pulses resulted in smaller synaptic potentials than were expected on the basis of summing the individual responses, consistent with the termination of both pathways onto a common population of neurons. Paired-pulse tests were then used to assess the effect of parasubicular stimulation on responses to piriform cortex stimulation. Responses of the entorhinal cortex to piriform cortex inputs were inhibited when the parasubiculum was stimulated 5 ms earlier and were enhanced when the parasubiculum was stimulated 20–150 ms earlier. These results indicate that excitatory inputs to the entorhinal cortex from the parasubiculum may enhance the propagation of neuronal activation patterns into the hippocampal circuit by increasing the responsiveness of the entorhinal cortex to appropriately timed inputs.



2019 ◽  
Author(s):  
Agrita Dubey ◽  
Supratim Ray

AbstractElectrocorticogram (ECoG), obtained from macroelectrodes placed on the cortex, is typically used in drug-resistant epilepsy patients, and is increasingly being used to study cognition in humans. These studies often use power in gamma (30-70 Hz) or high-gamma (>80 Hz) ranges to make inferences about neural processing. However, while the stimulus tuning properties of gamma/high-gamma power have been well characterized in local field potential (LFP; obtained from microelectrodes), analogous characterization has not been done for ECoG. Using a hybrid array containing both micro and ECoG electrodes implanted in the primary visual cortex of two female macaques, we compared the stimulus tuning preferences of gamma/high-gamma power in LFP versus ECoG and found them to be surprisingly similar. High-gamma power, thought to index the average firing rate around the electrode, was highest for the smallest stimulus (0.3° radius), and decreased with increasing size in both LFP and ECoG, suggesting local origins of both signals. Further, gamma oscillations were similarly tuned in LFP and ECoG to stimulus orientation, contrast and spatial frequency. This tuning was significantly weaker in electroencephalogram (EEG), suggesting that ECoG is more like LFP than EEG. Overall, our results validate the use of ECoG in clinical and basic cognitive research.



2017 ◽  
Vol 37 (33) ◽  
pp. 7962-7974 ◽  
Author(s):  
James E. Carmichael ◽  
Jimmie M. Gmaz ◽  
Matthijs A.A. van der Meer


2011 ◽  
Vol 105 (5) ◽  
pp. 2005-2017 ◽  
Author(s):  
Devarajan Sridharan ◽  
Kwabena Boahen ◽  
Eric I. Knudsen

Gamma-band (25–140 Hz) oscillations of the local field potential (LFP) are evoked by sensory stimuli in the mammalian forebrain and may be strongly modulated in amplitude when animals attend to these stimuli. The optic tectum (OT) is a midbrain structure known to contribute to multimodal sensory processing, gaze control, and attention. We found that presentation of spatially localized stimuli, either visual or auditory, evoked robust gamma oscillations with distinctive properties in the superficial (visual) layers and in the deep (multimodal) layers of the owl's OT. Across layers, gamma power was tuned sharply for stimulus location and represented space topographically. In the superficial layers, induced LFP power peaked strongly in the low-gamma band (25–90 Hz) and increased gradually with visual contrast across a wide range of contrasts. Spikes recorded in these layers included presumptive axonal (input) spikes that encoded stimulus properties nearly identically with gamma oscillations and were tightly phase locked with the oscillations, suggesting that they contribute to the LFP oscillations. In the deep layers, induced LFP power was distributed across the low and high (90–140 Hz) gamma-bands and tended to reach its maximum value at relatively low visual contrasts. In these layers, gamma power was more sharply tuned for stimulus location, on average, than were somatic spike rates, and somatic spikes synchronized with gamma oscillations. Such gamma synchronized discharges of deep-layer neurons could provide a high-resolution temporal code for signaling the location of salient sensory stimuli.



2018 ◽  
Vol 120 (3) ◽  
pp. 1090-1106 ◽  
Author(s):  
Bolesław L. Osinski ◽  
Alex Kim ◽  
Wenxi Xiao ◽  
Nisarg M. Mehta ◽  
Leslie M. Kay

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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