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.

Presynaptic Muscarinic Receptors Enhance Glutamate Release at the Mitral/Tufted to Granule Cell Dendrodendritic Synapse in the Rat Main Olfactory Bulb

2009 ◽  
Vol 101 (4) ◽  
pp. 2052-2061 ◽  
Author(s):  
Ambarish S. Ghatpande ◽  
Alan Gelperin
Keyword(s):  
Olfactory Bulb ◽  
Granule Cell ◽  
Basal Forebrain ◽  
Granule Cells ◽  
Calcium Influx ◽  
Glutamate Release ◽  
Gaba Release ◽  
Cellular Mechanisms ◽  
Tufted Cells

The mammalian olfactory bulb receives multiple modulatory inputs, including a cholinergic input from the basal forebrain. Understanding the functional roles played by the cholinergic input requires an understanding of the cellular mechanisms it modulates. In an in vitro olfactory bulb slice preparation we demonstrate cholinergic muscarinic modulation of glutamate release onto granule cells that results in γ-aminobutyric acid (GABA) release onto mitral/tufted cells. We demonstrate that the broad-spectrum cholinergic agonist carbachol triggers glutamate release from mitral/tufted cells that activates both AMPA and NMDA receptors on granule cells. Activation of the granule cell glutamate receptors leads to calcium influx through voltage-gated calcium channels, resulting in spike-independent, asynchronous GABA release at reciprocal dendrodendritic synapses that granule cells form with mitral/tufted cells. This cholinergic modulation of glutamate release persists through much of postnatal bulbar development, suggesting a functional role for cholinergic inputs from the basal forebrain in bulbar processing of olfactory inputs and possibly in postnatal development of the olfactory bulb.

Multiple site optical recording of transmembrane voltage (MSORTV), single-unit recordings, and evoked field potentials from the olfactory bulb of skate (Raja erinacea)

1990 ◽  
Vol 64 (6) ◽  
pp. 1767-1790 ◽  
Author(s):  
A. R. Cinelli ◽  
B. M. Salzberg
Keyword(s):  
Olfactory Bulb ◽  
Slow Component ◽  
Field Potential ◽  
Olfactory Nerve ◽  
Optical Signal ◽  
Nerve Fibers ◽  
Optical Recording ◽  
Transmembrane Voltage ◽  
N2 Wave

1. Multiple site optical recording of transmembrane voltage (MSORTV), together with conventional extracellular electrophysiological techniques were utilized with in vivo and in vitro preparations of the olfactory bulb of the Atlantic skate Raja erinacea to analyze electrical activity simultaneously in layers deep to the glomerular layer. 2. In the living animals and the in vitro isolated olfactory bulb, orthodromic stimulation evoked a compound action potential in the olfactory nerve fibers, followed by a series of early field-potential waves (N1, P1, N2, P2, N3, and N4). During paired stimulation experiments, unusual patterns of facilitation and suppression were observed for the N2 wave. 3. After orthodromic stimulation, single units, presumably mitral/tufted cells, exhibited a period of early discharge, followed by a period of suppression of spontaneous activity and of their test response in a pair stimulation paradigm. Some neurons also exhibited a labile period of reexcitation that was accompanied by a late surface negative field potential; these responses were also present in olfactory bulb slices. 4. Extrinsic absorption changes obtained from 500-microns saggital slices of the olfactory bulb, stained with the pyrazooxonal dye RH-155, consisted mainly of two types of depolarizing responses, a fast and a slow component, followed under some conditions by a late hyperpolarization. All signals exhibited wavelength dependences typical of the action spectrum of RH-155 and were abolished in the presence of tetrodotoxin (TTX) or high K+ in the bath. 5. The fast component of the optical signal represents synchronous compound action potentials conducted by the olfactory nerve fibers or evoked in the mitral/tufted somata and axonal pathways. The slow depolarizing optical signal appeared, after orthodromic stimuli, mainly in the zone between the glomeruli and the mitral/tufted layer; barium (1–10 mM), which depolarizes glial cells, increased its size and duration, suggesting that this signal does not reflect a glial response to [K+]o. 6. Different condition/test (C/T) intervals produced partial or complete suppression of the test response, depending on the recording site and the stimulus intensity. Just threshold orthodromic stimuli evoked an intermediate period of facilitation of the slow signals. A similar period was also observed in the N2 wave of the field potential. 7. Calcium channel blockers such as cadmium ion, or a low Ca2+ medium, suppressed the slow optical component whether evoked by orthodromic, antidromic, or direct stimulation. gamma-Aminobutyric acid (GABA) and baclofen also reduced or blocked the slow component of the extrinsic absorption signal.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Presynaptic and Postsynaptic NMDA Receptors Mediate Distinct Effects of Brain-Derived Neurotrophic Factor on Synaptic Transmission

2008 ◽  
Vol 100 (6) ◽  
pp. 3175-3184 ◽  
Author(s):  
Joseph C. Madara ◽  
Eric S. Levine
Keyword(s):  
Synaptic Transmission ◽  
Nmda Receptors ◽  
Neurotrophic Factor ◽  
Developmental Plasticity ◽  
Granule Cells ◽  
Slow Component ◽  
Glutamate Release ◽  
Brain Slices ◽  
Brain Derived Neurotrophic Factor ◽  
Cellular Mechanisms

In addition to its effects on neuronal survival and differentiation, brain-derived neurotrophic factor (BDNF) plays an important role in modulating synaptic transmission and plasticity in many brain areas, most notably the neocortex and hippocampus. These effects may underlie a role for BDNF in learning and memory as well as developmental plasticity. Consistent with localization of the tropomyosin-related kinase B receptor to both sides of the synapse, BDNF appears to have pre- and postsynaptic effects, but the underlying cellular mechanisms are unclear and it is not known whether pre- and postsynaptic modulations by BDNF occur simultaneously. To address these issues, we recorded dual-component (α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid [AMPA] and N-methyl-d-aspartate [NMDA]) miniature excitatory postsynaptic currents (mEPSCs) from cortical and hippocampal pyramidal neurons and dentate gyrus granule cells from acute brain slices. BDNF had no effect on the fast component of mEPSC decay or on the peak amplitude, suggesting that BDNF did not modulate postsynaptic AMPA receptors, although BDNF rapidly modulated NMDA receptors, as seen by an enhancement of the slow component of mEPSC decay that was prevented by blocking postsynaptic NMDA receptors. At the same time, BDNF acted presynaptically to enhance mEPSC frequency. Surprisingly, the effect on frequency was also NMDA receptor dependent, but required activation of presynaptic, not postsynaptic, NMDA receptors. BDNF also enhanced action potential–dependent glutamate release via presynaptic NMDA receptors, an effect that was unmasked when voltage-gated calcium channels were partially inhibited. Our results indicate that BDNF acutely modulates presynaptic release and postsynaptic responsiveness through simultaneous effects on pre- and postsynaptic NMDA receptors.

Neuromodulatory Effect of GnRH on the Synaptic Transmission of the Olfactory Bulbar Neural Circuit in Goldfish, Carassius auratus

2010 ◽  
Vol 104 (6) ◽  
pp. 3540-3550 ◽  
Author(s):  
Takafumi Kawai ◽  
Hideki Abe ◽  
Yasuhisa Akazome ◽  
Yoshitaka Oka
Keyword(s):  
Carassius Auratus ◽  
Neural Circuits ◽  
Neural Circuit ◽  
Granule Cells ◽  
Glutamate Release ◽  
Sensory Information ◽  
Field Potential ◽  
Field Potentials ◽  
Goldfish Carassius Auratus

Gonadotropin-releasing hormone (GnRH) is well known as a hypophysiotropic hormone that is produced in the hypothalamus and facilitates the release of gonadotropins from the pituitary gonadotropes. On the other hand, the functions of extrahypothalamic GnRH systems still remain elusive. Here we examined whether the activity of the olfactory bulbar neural circuits is modulated by GnRH that originates mainly from the terminal nerve (TN) GnRH system in goldfish ( Carassius auratus). As the morphological basis, we first observed that goldfish TNs mainly express salmon GnRH (sGnRH) mRNA and that sGnRH-immunoreactive fibers are distributed in both the mitral and the granule cell layers. We then examined by extracellular recordings the effect of GnRH on the electrically evoked in vitro field potentials that arise from synaptic activities from mitral to granule cells. We found that GnRH enhances the amplitude of the field potentials. Furthermore, these effects were observed in both cases when the field potentials were evoked by stimulating either the lateral or the medial olfactory tract, conveying functionally different sensory information, separately, and suggesting that GnRH may modulate the responsiveness to wide categories of odorants in the olfactory bulb. Because GnRH also changed the paired-pulse ratio, it is suggested that the increased amplitude of the field potential results from changes in the presynaptic glutamate release of mitral cells rather than the increase in the glutamate receptor sensitivity of granule cells. These results suggest that TN regulates the olfactory responsiveness of animals appropriately by releasing sGnRH peptides in the olfactory bulbar neural circuits.

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.

scholarly journals Transient Activity Induces a Long-Lasting Increase in the Excitability of Olfactory Bulb Interneurons

2008 ◽  
Vol 99 (1) ◽  
pp. 187-199 ◽  
Author(s):  
Tsuyoshi Inoue ◽  
Ben W. Strowbridge
Keyword(s):  
Olfactory Bulb ◽  
Granule Cells ◽  
Receptor Activation ◽  
Brain Regions ◽  
Persistent Activity ◽  
Cellular Mechanisms ◽  
Calcium Dependent ◽  
Transient Activity ◽  
Olfactory Bulb Slices ◽  
Processing And Storage

Little is known about the cellular mechanisms that underlie the processing and storage of sensory in the mammalian olfactory system. Here we show that persistent spiking, an activity pattern associated with working memory in other brain regions, can be evoked in the olfactory bulb by stimuli that mimic physiological patterns of synaptic input. We find that brief discharges trigger persistent activity in individual interneurons that receive slow, subthreshold oscillatory input in acute rat olfactory bulb slices. A 2- to 5-Hz oscillatory input, which resembles the synaptic drive that the olfactory bulb receives during sniffing, is required to maintain persistent firing. Persistent activity depends on muscarinic receptor activation and results from interactions between calcium-dependent afterdepolarizations and low-threshold Ca spikes in granule cells. Computer simulations suggest that intrinsically generated persistent activity in granule cells can evoke correlated spiking in reciprocally connected mitral cells. The interaction between the intrinsic currents present in reciprocally connected olfactory bulb neurons constitutes a novel mechanism for synchronized firing in subpopulations of neurons during olfactory processing.

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)

Features of Neuronal Synchrony in Mouse Visual Cortex

2003 ◽  
Vol 90 (2) ◽  
pp. 1115-1123 ◽  
Author(s):  
Gabriele Nase ◽  
Wolf Singer ◽  
Hannah Monyer ◽  
Andreas K. Engel
Keyword(s):  
Visual Cortex ◽  
Field Potential ◽  
Response Modulation ◽  
Temporal Patterning ◽  
Cellular Mechanisms ◽  
Neuronal Synchrony ◽  
Significant Difference ◽  
Random Dot Patterns

Synchronization of neuronal discharges has been hypothesized to play a role in defining cell assemblies representing particular constellations of stimulus features. In many systems and species, synchronization is accompanied by an oscillatory response modulation at frequencies in the γ-band. The cellular mechanisms underlying these phenomena of synchronization and oscillatory patterning have been studied mainly in vitro due to the difficulty in designing a direct in vivo assay. With the prospect of using conditional genetic manipulations of cortical network components, our objective was to test whether the mouse would meet the criteria to provide a model system for the study of γ-band synchrony. Multi-unit and local field potential recordings were made from the primary visual cortex of anesthetized C57BL/6J mice. Neuronal responses evoked by moving gratings, bars, and random dot patterns were analyzed with respect to neuronal synchrony and temporal patterning. Oscillations at γ-frequencies were readily evoked with all types of stimuli used. Oscillation and synchronization strength were largest for gratings and decreased when the noise level was increased in random-dot patterns. The center peak width of cross-correlograms was smallest for bars and increased with noise, yielding a significant difference between coherent random dot patterns versus patterns with 70% noise. Field potential analysis typically revealed increases of power in the γ-band during response periods. Our findings are compatible with a role for neuronal synchrony in mediating perceptual binding and suggest the usefulness of the mouse model for testing hypotheses concerning both the mechanisms and the functional role of temporal patterning.

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 DL-3-n-butylphthalide enhances synaptic plasticity in mouse model of brain impairments

STEMedicine ◽  
2022 ◽  
Vol 3 (1) ◽  
pp. e113
Author(s):  
Qian Ding ◽  
Qian Yu ◽  
Lei Tao ◽  
Yifei Guo ◽  
Juan Zhao ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Nmda Receptor ◽  
Glutamate Release ◽  
Field Potential ◽  
Nmda Receptor Subunits ◽  
Glutamate Level ◽  
Regulatory Effects ◽  
Glutaminase Activity

Synaptic impairment results in cognitive dysfunction of Alzheimer’s disease (AD). As a plant extract, it is found that DL-3-n-butylphthalide (L-NBP) rescues abnormal cognitive behaviors in AD animals. However, the regulatory effects of L-NBP on synaptic plasticity remains unclear. APP/PS1 mice at 12 months old received oral L-NBP treatment for 12 weeks. A water maze test assessed cognitive performances. In vitro patch-clamp recordings and in vivo field potential recordings were performed to evaluate synaptic plasticity. The protein expression of AMPA receptor subunits (GluR1 and GluR2) and NMDA receptor subunits (NR1, NR2A, and NR2B) was examined by Western blot. In addition, glutaminase activity and glutamate level in the hippocampus were measured by colorimetry to evaluate presynaptic glutamate release. L-NBP treatment could significantly improve learning and memory ability, upregulate NR2A and NR2B protein expressions, increase glutaminase activity and glutamate level in the hippocampus, and attenuate synaptic impairment transmission in the AD mice. L-NPB plays a beneficial role in AD mice by regulating NMDA receptor subunits’ expression and regulating presynaptic glutamate release.

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