Long-Term Enhancement of Synchronized Oscillations by Adrenergic Receptor Activation in the Olfactory Bulb

2008 ◽  
Vol 99 (4) ◽  
pp. 2021-2025 ◽  
Author(s):  
David H. Gire ◽  
Nathan E. Schoppa
Keyword(s):  
Olfactory Bulb ◽  
Associative Learning ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Olfactory Nerve ◽  
Receptor Activation ◽  
Cell Network ◽  
Functional Perspective ◽  
Gamma Frequency

The noradrenergic system is widely thought to be important for associative learning in the olfactory system through actions in the first processing structure, the main olfactory bulb (MOB). Here, we used extracellular local field potential (LFP) and patch-clamp recordings in rat MOB slices to examine norepinephrine (NE)-induced long-term changes in circuit properties that might underlie learning. During responses to patterned olfactory nerve stimulation mimicking the breathing cycle, NE induced a long-term increase in gamma frequency (30–70 Hz) synchronized oscillations. The enhancement persisted long after washout of NE (≤70 min), depended on the combined actions of NE and neuronal stimulation, and seemed to be caused by enhanced excitatory drive on the mitral/granule cell network that underlies rapid gamma oscillations. The last effect, increased excitation, was manifested as an increase in evoked long-lasting depolarizations (LLDs) in mitral cells. From a functional perspective, the observed long-term cellular and network changes could promote associative learning by amplifying odor-specific signals.

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

2016 ◽  
Vol 116 (2) ◽  
pp. 522-539 ◽  
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.

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 Adrenergic Receptor-Mediated Disinhibition of Mitral Cells Triggers Long-Term Enhancement of Synchronized Oscillations in the Olfactory Bulb

2010 ◽  
Vol 104 (2) ◽  
pp. 665-674 ◽  
Author(s):  
Sruthi Pandipati ◽  
David H. Gire ◽  
Nathan E. Schoppa
Keyword(s):  
Olfactory Bulb ◽  
Granule Cells ◽  
Gamma Oscillations ◽  
Olfactory Learning ◽  
Inhibitory Synapses ◽  
Mitral Cells ◽  
Acute Effects ◽  
Long Term Effects ◽  
Gamma Frequency

Norepinephrine (NE) is widely implicated in various forms of associative olfactory learning in rodents, including early learning preference in neonates. Here we used patch-clamp recordings in rat olfactory bulb slices to assess cellular actions of NE, examining both acute, short-term effects of NE as well as the relationship between these acute effects and long-term cellular changes that could underlie learning. Our focus for long-term effects was on synchronized gamma frequency (30–70 Hz) oscillations, shown in prior studies to be enhanced for up to an hour after brief exposure of a bulb slice to NE and neuronal stimulation. In terms of acute effects, we found that a dominant action of NE was to reduce inhibitory GABAergic transmission from granule cells (GCs) to output mitral cells (MCs). This disinhibition was also induced by clonidine, an agonist specific for α2 adrenergic receptors (ARs). Acute NE-induced disinhibition of MCs appeared to be linked to long-term enhancement of gamma oscillations, based, first, on the fact that clonidine, but not agonists specific for other AR subtypes, mimicked NE's long-term actions. In addition, the α2 AR-specific antagonist yohimbine blocked the long-term enhancement of the oscillations due to NE. Last, brief exposure of the slice to the GABAA receptor antagonist gabazine, to block inhibitory synapses directly, also induced the long-term changes. Acute disinhibition is a plausible permissive effect of NE leading to olfactory learning, because, when combined with exposure to a specific odor, it should lead to neuron-specific increases in intracellular calcium of the type generally associated with long-term synaptic modifications.

Dopamine D2 Receptor–Mediated Presynaptic Inhibition of Olfactory Nerve Terminals

2001 ◽  
Vol 86 (6) ◽  
pp. 2986-2997 ◽  
Author(s):  
Matthew Ennis ◽  
Fu-Ming Zhou ◽  
Kelly J. Ciombor ◽  
Vassiliki Aroniadou-Anderjaska ◽  
Abdallah Hayar ◽  
...  
Keyword(s):  
Olfactory Bulb ◽  
Dopamine D2 Receptor ◽  
Signal Transmission ◽  
D2 Receptor ◽  
Field Potential ◽  
Olfactory Nerve ◽  
D2 Receptors ◽  
Receptor Subtype ◽  
Juxtaglomerular Cells ◽  
Synaptic Responses

Olfactory receptor neurons of the nasal epithelium project via the olfactory nerve (ON) to the glomeruli of the main olfactory bulb, where they form glutamatergic synapses with the apical dendrites of mitral and tufted cells, the output cells of the olfactory bulb, and with juxtaglomerular interneurons. The glomerular layer contains one of the largest population of dopamine (DA) neurons in the brain, and DA in the olfactory bulb is found exclusively in juxtaglomerular neurons. D2 receptors, the predominant DA receptor subtype in the olfactory bulb, are found in the ON and glomerular layers, and are present on ON terminals. In the present study, field potential and single-unit recordings, as well as whole cell patch-clamp techniques, were used to investigate the role of DA and D2 receptors in glomerular synaptic processing in rat and mouse olfactory bulb slices. DA and D2 receptor agonists reduced ON-evoked synaptic responses in mitral/tufted and juxtaglomerular cells. Spontaneous and ON-evoked spiking of mitral cells was also reduced by DA and D2 agonists, and enhanced by D2 antagonists. DA did not produce measurable postsynaptic changes in juxtaglomerular cells, nor did it alter their responses to mitral/tufted cell inputs. DA also reduced 1) paired-pulse depression of ON-evoked synaptic responses in mitral/tufted and juxtaglomerular cells and 2) the amplitude and frequency of spontaneous, but not miniature, excitatory postsynaptic currents in juxtaglomerular cells. Taken together, these findings are consistent with the hypothesis that activation of D2 receptors presynaptically inhibits ON terminals. DA and D2 agonists had no effect in D2 receptor knockout mice, suggesting that D2 receptors are the only type of DA receptors that affect signal transmission from the ON to the rodent olfactory bulb.

A Study of Terminal Degeneration in the Olfactory Bulb of the Rat

1972 ◽  
Vol 10 (3) ◽  
pp. 585-619
Author(s):  
A. J. PINCHING ◽  
T. P. S. POWELL
Keyword(s):  
Olfactory Bulb ◽  
Synaptic Cleft ◽  
Olfactory Nerve ◽  
Synaptic Membrane ◽  
Morphological Identification ◽  
Axon Terminals ◽  
Quantitative Characteristics ◽  
Terminal Degeneration ◽  
Qualitative And Quantitative Characteristics

An ultrastructural study of degeneration in axon terminals of the glomerular layer of the rat olfactory bulb is described, concentrating particularly on the sequence of degeneration in the olfactory nerve terminals and the long-term events in the degeneration process in several terminal types. Olfactory nerve terminal degeneration is divided into 5 stages, representing parts of the sequential changes taking place in the terminal after fibre section. The main features in the sequence are as follows: I. Swelling of the terminal and its vesicles. II. Initial shrinkage of the terminal, while vesicles remain swollen and some are distorted. III. Further shrinkage and darkening of the terminal, distortion of many of the vesicles and some mitochondrial swelling. IV. Extreme shrinkage of the terminal and loss of cytoplasmic detail; synaptic contact still intact or partially separated. V. Disappearance of the presynaptic terminal and persistence of the post-synaptic thickening. The validity of the observation of the persistence of post-synaptic membrane thickenings is considered and evidence adduced in its favour, both qualitative and quantitative. Characteristics of the newly apposed profiles are described, including cisternae and alveolate vesicles; the extracellular material of the synaptic cleft is considered in the light of its association with persisting thickenings. The relevance of these associated Structures is discussed in terms of function and development. Spontaneous degeneration of olfactory nerves and the degeneration of the vomeronasal nerves in the accessory olfactory bulb are described, as well as Stage V in the degeneration of other terminal types of the glomeruli, following various lesions; persistence of post-synaptic thickenings after the degeneration of terminals showing symmetrical membrane thickenings is included. Observations on the persistence of post-synaptic thickenings in various sites in the central and peripheral nervous systems are reviewed in the context of the present study; the problems arising out of the morphological identification of apposition or reinnervations are discussed.

Dendritic origin of late events in optical recordings from salamander olfactory bulb

1992 ◽  
Vol 68 (3) ◽  
pp. 786-806 ◽  
Author(s):  
A. R. Cinelli ◽  
B. M. Salzberg
Keyword(s):  
Olfactory Bulb ◽  
Time Course ◽  
Slow Component ◽  
Field Potential ◽  
Olfactory Nerve ◽  
Nerve Fibers ◽  
Dependent Manner ◽  
Gamma Aminobutyric Acid ◽  
Direct Stimulation ◽  
Compound Action

1. Optical recordings of membrane-potential changes were used to characterize the origin and properties of the electrical signals from the dendritic level in slices of the salamander olfactory bulb. 2. The optical events were correlated with field-potential waves recorded simultaneously. Both responses exhibited patterns similar to those found in other species. 3. Orthodromic stimulation evoked a compound action potential in the olfactory nerve fibers, followed by two additional principal waves (N1 and N2). These field-potential waves reflected excitatory postsynaptic potentials at the primary mitral/tufted and granule cell dendrites, respectively. 4. Extrinsic optical signals from horizontal slices stained with the pyrazo-oxonal dye RH-155 showed a characteristic sequence of depolarizing and hyperpolarizing events. All of the signals exhibited a wavelength dependence expected for this dye and were abolished in the presence of high K+ in the bath. 5. According to their time courses, depolarizing responses under normal recording conditions were divided into two components, fast and slow. Orthodromic stimuli evoked a fast presynaptic response that represents synchronous compound action potentials from olfactory nerve fibers. At subglomerular levels, additional fast responses could often be recorded at the peri/subglomerular level and in the mitral/tufted somata region. These postsynaptic responses partially coincided with the rising phase of a different depolarizing signal, a slow component characterized by its prolonged time course. 6. With orthodromic stimulation, this slow signal attained its largest amplitude in the zone between the glomeruli and the superficial part of the external plexiform layer (EPL). Antidromic stimuli evoked a signal with some similarities to the one evoked orthodromically, but originating in deeper EPL regions. 7. Slow components were characterized by their Ca dependence. Low Ca2+ medium, or calcium channel blockers, suppressed this optical component, whether evoked orthodromically, antidromically, or by direct stimulation. In addition, Ba2+ (2.5–3.6 mM) in the bath did not abolish these responses, suggesting that they do not reflect a glial depolarization in response to elevated extracellular K+ concentration ([K+]o). 8. Locally applied stimuli next to the glomerular layer elicited these signals in 5–10 microM tetrodotoxin (TTX) or in low extracellular Na+ concentration ([Na+]o) medium, but antidromic or orthodromic stimuli failed to evoke the response under these conditions. The sizes of the responses to local stimuli remained constant, but an increase in their duration was observed in either TTX or low [Na+]o. 9. gamma-Aminobutyric acid (GABA) and baclofen reduced the size of the slow components in a dose-dependent manner.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Sniff-Like Patterned Input Results in Long-Term Plasticity at the Rat Olfactory Bulb Mitral and Tufted Cell to Granule Cell Synapse

2016 ◽  
Vol 2016 ◽  
pp. 1-16 ◽  
Author(s):  
Mahua Chatterjee ◽  
Fernando Perez de los Cobos Pallares ◽  
Alex Loebel ◽  
Michael Lukas ◽  
Veronica Egger
Keyword(s):  
Olfactory Bulb ◽  
Granule Cells ◽  
Brain Slices ◽  
Long Term Potentiation ◽  
Receptor Activation ◽  
Term Potentiation ◽  
Presynaptic Release ◽  
Extra Activity ◽  
Hippocampal Theta

During odor sensing the activity of principal neurons of the mammalian olfactory bulb, the mitral and tufted cells (MTCs), occurs in repetitive bursts that are synchronized to respiration, reminiscent of hippocampal theta-gamma coupling. Axonless granule cells (GCs) mediate self- and lateral inhibitory interactions between the excitatory MTCs via reciprocal dendrodendritic synapses. We have explored long-term plasticity at this synapse by using a theta burst stimulation (TBS) protocol and variations thereof. GCs were excited via glomerular stimulation in acute brain slices. We find that TBS induces exclusively long-term depression in the majority of experiments, whereas single bursts (“single-sniff paradigm”) can elicit both long-term potentiation and depression. Statistical analysis predicts that the mechanism underlying this bidirectional plasticity involves the proportional addition or removal of presynaptic release sites. Gamma stimulation with the same number of APs as in TBS was less efficient in inducing plasticity. Both TBS- and “single-sniff paradigm”-induced plasticity depend on NMDA receptor activation. Since the onset of plasticity is very rapid and requires little extra activity, we propose that these forms of plasticity might play a role already during an ongoing search for odor sources. Our results imply that components of both short-term and long-term olfactory memory may be encoded at this synapse.

scholarly journals Beyond spikes: Multiscale computational analysis of in vivo long-term recordings in the cockroach circadian clock

2019 ◽  
Vol 3 (4) ◽  
pp. 944-968 ◽  
Author(s):  
Pablo Rojas ◽  
Jenny A. Plath ◽  
Julia Gestrich ◽  
Bharath Ananthasubramaniam ◽  
Martin E. Garcia ◽  
...  
Keyword(s):  
Circadian Clock ◽  
Field Potential ◽  
Dynamic Features ◽  
Pigment Dispersing Factor ◽  
Gamma Frequency ◽  
Accessory Medulla ◽  
Electrophysiological Recordings ◽  
Wide Range

The circadian clock of the nocturnal Madeira cockroach is located in the accessory medulla, a small nonretinotopic neuropil in the brain’s visual system. The clock comprises about 240 neurons that control rhythms in physiology and behavior such as sleep-wake cycles. The clock neurons contain an abundant number of partly colocalized neuropeptides, among them pigment-dispersing factor (PDF), the insects’ most important circadian coupling signal that controls sleep-wake rhythms. We performed long-term loose-patch clamp recordings under 12:12-hr light-dark cycles in the cockroach clock in vivo. A wide range of timescales, from milliseconds to seconds, were found in spike and field potential patterns. We developed a framework of wavelet transform–based methods to detect these multiscale electrical events. We analyzed frequencies and patterns of events with interesting dynamic features, such as mixed-mode oscillations reminiscent of sharp-wave ripples. Oscillations in the beta/gamma frequency range (20–40 Hz) were observed to rise at dawn, when PDF is released, peaking just before the onset of locomotor activity of the nocturnal cockroach. We expect that in vivo electrophysiological recordings combined with neuropeptide/antagonist applications and behavioral analysis will determine whether specific patterns of electrical activity recorded in the network of the cockroach circadian clock are causally related to neuropeptide-dependent control of behavior.

Dopaminergic neuromodulation of synaptic transmission between mitral and granule cells in the teleost olfactory bulb

2012 ◽  
Vol 107 (5) ◽  
pp. 1313-1324 ◽  
Author(s):  
Takafumi Kawai ◽  
Hideki Abe ◽  
Yoshitaka Oka
Keyword(s):  
Olfactory Bulb ◽  
Synaptic Transmission ◽  
Granule Cells ◽  
Glutamate Release ◽  
Field Potential ◽  
Olfactory Nerve ◽  
Oscillatory Activity ◽  
Cellular Mechanisms ◽  
Olfactory Information

A growing body of evidence suggests that teleosts are important models for the study of neural processing of olfactory information, and the functional role of dopamine (DA), which is a potent neuromodulator endogenous to the mammalian olfactory bulb, has been one of the strongest focuses in this field. However, the cellular mechanisms of dopaminergic neuromodulation in olfactory bulbar neural circuits have not been fully understood. We investigated such mechanisms by using the goldfish, which offers several advantages for analyzing olfactory information processing by electrophysiological methods. First, we found in the olfactory bulb that numerous cell bodies of the dopaminergic neurons are mainly distributed in the mitral cell layer and extend fine processes to the glomerular layer. Next, we made in vitro field potential recordings and showed that synaptic transmissions from mitral to granule cells were suppressed by DA application. DA also increased the paired-pulse ratio, suggesting that the suppression of synaptic transmission is caused by a decrease in presynaptic glutamate release from the mitral cells. Furthermore, DA significantly suppressed the oscillatory activity of the olfactory bulb in response to olfactory stimuli. Although DA suppresses the synaptic inputs from the olfactory nerve to the olfactory bulbar neurons in mammals, this phenomenon was not observed in the goldfish. These findings indicate that suppression of the mitral to granule cell synaptic transmission in the reciprocal synapses plays an important role in the negative regulation of olfactory responsiveness in the goldfish olfactory bulb.

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