Aging Alters Olfactory Bulb Network Oscillations and Connectivity: Relevance for Aging-Related Neurodegeneration Studies

The aging process eventually cause a breakdown in critical synaptic plasticity and connectivity leading to deficits in memory function. The olfactory bulb (OB) and the hippocampus, both regions of the brain considered critical for the processing of odors and spatial memory, are commonly affected by aging. Using an aged wild-type C57B/6 mouse model, we sought to define the effects of aging on hippocampal plasticity and the integrity of cortical circuits. Specifically, we measured the long-term potentiation of high-frequency stimulation (HFS-LTP) at the Shaffer-Collateral CA1 pyramidal synapses. Next, local field potential (LFP) spectra, phase-amplitude theta-gamma coupling (PAC), and connectivity through coherence were assessed in the olfactory bulb, frontal and entorhinal cortices, CA1, and amygdala circuits. The OB of aged mice showed a significant increase in the number of histone H2AX-positive neurons, a marker of DNA damage. While the input-output relationship measure of basal synaptic activity was found not to differ between young and aged mice, a pronounced decline in the slope of field excitatory postsynaptic potential (fEPSP) and the population spike amplitude (PSA) were found in aged mice. Furthermore, aging was accompanied by deficits in gamma network oscillations, a shift to slow oscillations, reduced coherence and theta-gamma PAC in the OB circuit. Thus, while the basal synaptic activity was unaltered in older mice, impairment in hippocampal synaptic transmission was observed only in response to HFS. However, age-dependent alterations in neural network appeared spontaneously in the OB circuit, suggesting the neurophysiological basis of synaptic deficits underlying olfactory processing. Taken together, the results highlight the sensitivity and therefore potential use of LFP quantitative network oscillations and connectivity at the OB level as objective electrophysiological markers that will help reveal specific dysfunctional circuits in aging-related neurodegeneration studies.

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Functional Alterations in the Olfactory Neuronal Circuit Occur before Hippocampal Plasticity Deficits in the P301S Mouse Model of Tauopathy: Implications for Early Diagnosis and Translational Research in Alzheimer’s Disease

International Journal of Molecular Sciences ◽

10.3390/ijms21155431 ◽

2020 ◽

Vol 21 (15) ◽

pp. 5431

Author(s):

Abdallah Ahnaou ◽

Daniela Rodriguez-Manrique ◽

Ria Biermans ◽

Sofie Embrechts ◽

Nikolay V. Manyakov ◽

...

Keyword(s):

Alzheimer’S Disease ◽

Alzheimer's Disease ◽

Synaptic Transmission ◽

Long Term Potentiation ◽

Synaptic Activity ◽

Oscillatory Activity ◽

High Frequency Stimulation ◽

Excitatory Postsynaptic Potential ◽

Network Oscillations ◽

Significant Difference

Alzheimer’s disease (AD) is characterized by neuronal loss and impaired synaptic transmission, ultimately leading to cognitive deficits. Early in the disease, the olfactory track seems most sensitive to tauopathy, while most plasticity studies focused on the hippocampal circuits. Functional network connectivity (FC) and long-term potentiation (LTP), considered as the plasticity substrate of learning and memory, were longitudinally assessed in mice of the P301S model of tauopathy following the course (time and location) of progressively neurodegenerative pathology (i.e., at 3, 6, and 9 months of age) and in their wild type (WT) littermates. Using in vivo local field potential (LFP) recordings, early (at three months) dampening in the gamma oscillatory activity and impairments in the phase-amplitude theta-gamma coupling (PAC) were found in the olfactory bulb (OB) circuit of P301S mice, which were maintained through the whole course of pathology development. In contrast, LFP oscillatory activity and PAC indices were normal in the entorhinal cortex, hippocampal CA1 and CA3 nuclei. Field excitatory postsynaptic potential (fEPSP) recordings from the Shaffer collateral (SC)-CA1 hippocampal stratum pyramidal revealed a significant altered synaptic LTP response to high-frequency stimulation (HFS): at three months of age, no significant difference between genotypes was found in basal synaptic activity, while signs of a deficit in short term plasticity were revealed by alterations in the fEPSPs. At six months of age, a slight deviance was found in basal synaptic activity and significant differences were observed in the LTP response. The alterations in network oscillations at the OB level and impairments in the functioning of the SC-CA1 pyramidal synapses strongly suggest that the progression of tau pathology elicited a brain area, activity-dependent disturbance in functional synaptic transmission. These findings point to early major alterations of neuronal activity in the OB circuit prior to the disturbance of hippocampal synaptic plasticity, possibly involving tauopathy in the anomalous FC. Further research should determine whether those early deficits in the OB network oscillations and FC are possible mechanisms that potentially promote the emergence of hippocampal synaptic impairments during the progression of tauopathy.

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Metabotropic glutamate receptor dependent EPSP and EPSP-spike potentiation in area CA1 of the submerged rat hippocampal slice

Journal of Neurophysiology ◽

10.1152/jn.1996.76.5.3126 ◽

1996 ◽

Vol 76 (5) ◽

pp. 3126-3135 ◽

Cited By ~ 32

Author(s):

N. A. Breakwell ◽

M. J. Rowan ◽

R. Anwyl

Keyword(s):

Nmda Receptor ◽

Receptor Antagonist ◽

Cell Body ◽

Metabotropic Glutamate Receptor ◽

Long Term Potentiation ◽

High Frequency Stimulation ◽

Excitatory Postsynaptic Potential ◽

Area Ca1 ◽

Gabaa Receptor Antagonist

1. We reexamined the important areas of conflict in (1S,3R)-1-aminocyclopentane-1,3-dicarboxylic acid [(1S,3R)-ACPD]-induced potentiation of the field excitatory postsynaptic potential (EPSP) and, for the first time, investigated the role of mGluRs in EPSP-spike (E-S) coupling. 2. (1S,3R)-ACPD (10 microM) bath applied for 20 min consistently induced a long-lasting potentiation of the dendritic EPSP in area CA1 of submerged rat hippocampal slices, which was considerably faster in onset than described previously. 3. This effect was not associated with any change in presynaptic fiber volley but was dependent on both an intact CA3 connection, because removal of area CA3 blocked (1S,3R)-ACPD-induced potentiation, and also on functional N-methyl-D-aspartate (NMDA) receptors, because (1S,3R)-ACPD-induced potentiation was blocked by inclusion of the NMDA receptor antagonist D(-)-2-amino-5-phosphonopentanoic acid (AP5; 50 microM). 4. (1S,3R)-ACPD induced a long-lasting potentiation of the population spike (PS) amplitude that was consistently larger than that of the EPSP measured in the cell body area. This EPSP-PS (E-S) potentiation was blocked by inclusion of the gamma-aminobuturic acid-A (GABAA) receptor antagonist, picrotoxin (50 microM). 5. E-S potentiation induced by high-frequency stimulation (HFS), which was of the same magnitude as that induced by (1S,3R)-ACPD, was blocked by the mGluR-selective antagonist (+)-alpha-methyl-4-carboxyphenylglycine (+MCPG; 250 microM). +MCPG also blocked HFS-induced long-term potentiation (LTP) of the EPSP measured in the cell body. 6. These results suggest that (1S,3R)-ACPD-induced potentiation is NMDA receptor dependent, contrary to some previous findings, and provide further evidence that both synaptic and E-S potentiation induced by (1S,3R)-ACPD share common mechanisms of expression with HFS-induced LTP. The data emphasize the important role of mGluRs in induction of EPSP LTP and E-S potentiation.

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Psychosocial Crowding Stress-Induced Changes in Synaptic Transmission and Glutamate Receptor Expression in the Rat Frontal Cortex

Biomolecules ◽

10.3390/biom11020294 ◽

2021 ◽

Vol 11 (2) ◽

pp. 294

Author(s):

Agnieszka Zelek-Molik ◽

Bartosz Bobula ◽

Anna Gądek-Michalska ◽

Katarzyna Chorązka ◽

Adam Bielawski ◽

...

Keyword(s):

Frontal Cortex ◽

Primary Motor Cortex ◽

Interleukin 1 ◽

Field Potential ◽

Long Term Potentiation ◽

Plasma Corticosterone ◽

Receptor Expression ◽

Synaptic Activity ◽

Common Mechanism ◽

Crowding Stress

This study demonstrates how exposure to psychosocial crowding stress (CS) for 3, 7, and 14 days affects glutamate synapse functioning and signal transduction in the frontal cortex (FC) of rats. CS effects on synaptic activity were evaluated in FC slices of the primary motor cortex (M1) by measuring field potential (FP) amplitude, paired-pulse ratio (PPR), and long-term potentiation (LTP). Protein expression of GluA1, GluN2B mGluR1a/5, VGLUT1, and VGLUT2 was assessed in FC by western blot. The body’s response to CS was evaluated by measuring body weight and the plasma level of plasma corticosterone (CORT), adrenocorticotropic hormone (ACTH), and interleukin 1 beta (IL1B). CS 3 14d increased FP and attenuated LTP in M1, while PPR was augmented in CS 14d. The expression of GluA1, GluN2B, and mGluR1a/5 was up-regulated in CS 3d and downregulated in CS 14d. VGLUTs expression tended to increase in CS 7d. The failure to blunt the effects of chronic CS on FP and LTP in M1 suggests the impairment of habituation mechanisms by psychosocial stressors. PPR augmented by chronic CS with increased VGLUTs level in the CS 7d indicates that prolonged CS exposure changed presynaptic signaling within the FC. The CS bidirectional profile of changes in glutamate receptors’ expression seems to be a common mechanism evoked by stress in the FC.

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Distance-Dependent Ni2+-Sensitivity of Synaptic Plasticity in Apical Dendrites of Hippocampal CA1 Pyramidal Cells

Journal of Neurophysiology ◽

10.1152/jn.00536.2001 ◽

2002 ◽

Vol 87 (2) ◽

pp. 1169-1174 ◽

Cited By ~ 29

Author(s):

Yoshikazu Isomura ◽

Yoko Fujiwara-Tsukamoto ◽

Michiko Imanishi ◽

Atsushi Nambu ◽

Masahiko Takada

Keyword(s):

Calcium Influx ◽

Critical Role ◽

Field Potential ◽

Pyramidal Cells ◽

Long Term Potentiation ◽

Apical Dendrite ◽

Excitatory Postsynaptic Potential ◽

Distal Dendrite ◽

Ca1 Pyramidal Cells ◽

Hippocampal Ca1

Low concentration of Ni2+, a T- and R-type voltage-dependent calcium channel (VDCC) blocker, is known to inhibit the induction of long-term potentiation (LTP) in the hippocampal CA1 pyramidal cells. These VDCCs are distributed more abundantly at the distal area of the apical dendrite than at the proximal dendritic area or soma. Therefore we investigated the relationship between the Ni2+-sensitivity of LTP induction and the synaptic location along the apical dendrite. Field potential recordings revealed that 25 μM Ni2+ hardly influenced LTP at the proximal dendritic area (50 μm distant from the somata). In contrast, the same concentration of Ni2+ inhibited the LTP induction mildly at the middle dendritic area (150 μm) and strongly at the distal dendritic area (250 μm). Ni2+ did not significantly affect either the synaptic transmission at the distal dendrite or the burst-firing ability at the soma. However, synaptically evoked population spikes recorded near the somata were slightly reduced by Ni2+ application, probably owing to occlusion of dendritic excitatory postsynaptic potential (EPSP) amplification. Even when the stimulating intensity was strengthened sufficiently to overcome such a reduction in spike generation during LTP induction, the magnitude of distal LTP was not significantly recovered from the Ni2+-dependent inhibition. These results suggest that Ni2+ may inhibit the induction of distal LTP directly by blocking calcium influx through T- and/or R-type VDCCs. The differentially distributed calcium channels may play a critical role in the induction of LTP at dendritic synapses of the hippocampal pyramidal cells.

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Partial Disinhibition Is Required for Transition of Stimulus-Induced Sharp Wave–Ripple Complexes Into Recurrent Epileptiform Discharges in Rat Hippocampal Slices

Journal of Neurophysiology ◽

10.1152/jn.00186.2010 ◽

2011 ◽

Vol 105 (1) ◽

pp. 172-187 ◽

Cited By ~ 30

Author(s):

Agustin Liotta ◽

Gürsel Çalışkan ◽

Rizwan ul Haq ◽

Jan O. Hollnagel ◽

Anton Rösler ◽

...

Keyword(s):

Hippocampal Slices ◽

Field Potential ◽

Long Term Potentiation ◽

Equilibrium Potential ◽

High Frequency Stimulation ◽

Extracellular Potassium ◽

Epileptogenic Zone ◽

Sharp Wave ◽

Epileptiform Discharges ◽

Inhibitory Conductance

Sharp wave–ripple complexes (SPW-Rs) in the intact rodent hippocampus are characterized by slow field potential transients superimposed by close to 200-Hz ripple oscillations. Similar events have been recorded in hippocampal slices where SPW-Rs occur spontaneously or can be induced by repeated application of high-frequency stimulation, a standard protocol for induction of long-lasting long-term potentiation. Such stimulation is reminiscent of protocols used to induce kindling epilepsy and ripple oscillations may be predictive of the epileptogenic zone in temporal lobe epilepsy. In the present study, we investigated the relation between recurrent epileptiform discharges (REDs) and SPW-Rs by studying effects of partial removal of inhibition. In particular, we compared the effects of nicotine, low-dose bicuculline methiodide (BMI), and elevated extracellular potassium concentration ([K+]o) on induced SPW-Rs. We show that nicotine dose-dependently transformed SPW-Rs into REDs. This transition was associated with reduced inhibitory conductance in CA3 pyramidal cells. Similar results were obtained from slices where the GABAergic conductance was reduced by application of low concentrations of BMI (1–2 μM). In contrast, sharp waves were diminished by phenobarbital. Elevating [K+]o from 3 to 8.5 mM did not transform SPW-Rs into REDs but significantly increased their incidence and amplitude. Under these conditions, the equilibrium potential for inhibition was shifted in depolarizing direction, whereas inhibitory conductance was significantly increased. Interestingly, the propensity of elevated [K+]o to induce seizure-like events was reduced in slices where SPW-Rs had been induced. In conclusion, recruitment of inhibitory cells during SPW-Rs may serve as a mechanism by which hyperexcitation and eventually seizure generation might be prevented.

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Impact of Time-Dependent Changes in Spine Density and Spine Shape on the Input-Output Properties of a Dendritic Branch: A Computational Study

Journal of Neurophysiology ◽

10.1152/jn.00373.2004 ◽

2005 ◽

Vol 93 (4) ◽

pp. 2073-2089 ◽

Cited By ~ 23

Author(s):

D. W. Verzi ◽

M. B. Rheuben ◽

S. M. Baer

Keyword(s):

Computational Study ◽

Long Term Potentiation ◽

Synaptic Activity ◽

High Frequency Stimulation ◽

Spine Density ◽

Dendritic Branch ◽

Input Output ◽

Stem Resistance ◽

Rate Of Increase ◽

Activity Dependent

Populations of dendritic spines can change in number and shape quite rapidly as a result of synaptic activity. Here, we explore the consequences of such changes on the input–output properties of a dendritic branch. We consider two models: one for activity-dependent spine densities and the other for calcium-mediated spine-stem restructuring. In the activity-dependent density model we find that for repetitive synaptic input to passive spines, changes in spine density remain local to the input site. For excitable spines, the spine density increases both inside and outside the input region. When the spine stem resistances are relatively high, the transition to higher dendritic output is abrupt; when low, the rate of increase is gradual and resembles long-term potentiation. In the second model, spine density is held constant, but the stem dimensions are allowed to change as a result of stimulation-induced calcium influxes. The model is formulated so that a moderate amount of synaptic activation results in spine stem elongation, whereas high levels of activation result in stem shortening. Under these conditions, passive spines receiving modest stimulation progressively increase their spine stem resistance and head potentials, but little change occurs in the dendritic output. For excitable spines, modest stimulation frequencies cause a lengthening of both stimulated and neighboring spines and the stimulus eventually propagates. High-frequency stimulation that causes spines to shorten in the stimulated region decreases the amplitude of the dendritic output slightly or drastically, depending on initial spine densities and stem resistances.

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Irradiation of the Juvenile Brain Provokes a Shift from Long-Term Potentiation to Long-Term Depression

Developmental Neuroscience ◽

10.1159/000430435 ◽

2015 ◽

Vol 37 (3) ◽

pp. 263-272 ◽

Cited By ~ 4

Author(s):

Giulia Zanni ◽

Kai Zhou ◽

Ilse Riebe ◽

Cuicui Xie ◽

Changlian Zhu ◽

...

Keyword(s):

Synaptic Plasticity ◽

Young Patients ◽

Long Term Potentiation ◽

Hippocampal Neurogenesis ◽

Adult Brain ◽

High Frequency Stimulation ◽

Excitatory Postsynaptic Potential ◽

Long Term Depression ◽

Term Potentiation

Radiotherapy is common in the treatment of brain tumors in children but often causes deleterious, late-appearing sequelae, including cognitive decline. This is thought to be caused, at least partly, by the suppression of hippocampal neurogenesis. However, the changes in neuronal network properties in the dentate gyrus (DG) following the irradiation of the young, growing brain are still poorly understood. We characterized the long-lasting effects of irradiation on the electrophysiological properties of the DG after a single dose of 6-Gy whole-brain irradiation on postnatal day 11 in male Wistar rats. The assessment of the basal excitatory transmission in the medial perforant pathway (MPP) by an examination of the field excitatory postsynaptic potential/volley ratio showed an increase of the synaptic efficacy per axon in irradiated animals compared to sham controls. The paired-pulse ratio at the MPP granule cell synapses was not affected by irradiation, suggesting that the release probability of neurotransmitters was not altered. Surprisingly, the induction of long-term synaptic plasticity in the DG by applying 4 trains of high-frequency stimulation provoked a shift from long-term potentiation (LTP) to long-term depression (LTD) in irradiated animals compared to sham controls. The morphological changes consisted in a virtually complete ablation of neurogenesis following irradiation, as judged by doublecortin immunostaining, while the inhibitory network of parvalbumin interneurons was intact. These data suggest that the irradiation of the juvenile brain caused permanent changes in synaptic plasticity that would seem consistent with an impairment of declarative learning. Unlike in our previous study in mice, lithium treatment did unfortunately not ameliorate any of the studied parameters. For the first time, we show that the effects of cranial irradiation on long-term synaptic plasticity is different in the juvenile compared with the adult brain, such that while irradiation of the adult brain will only cause a reduction in LTP, irradiation of the juvenile brain goes further and causes LTD. Although the mechanisms underlying the synaptic alterations need to be elucidated, these findings provide a better understanding of the effects of irradiation in the developing brain and the cognitive deficits observed in young patients who have been subjected to cranial radiotherapy.

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Interaction Between Tetanus Long-Term Potentiation and Hypoxia-Induced Potentiation in the Rat Hippocampus

Journal of Neurophysiology ◽

10.1152/jn.1997.78.5.2475 ◽

1997 ◽

Vol 78 (5) ◽

pp. 2475-2482 ◽

Cited By ~ 18

Author(s):

M. Lyubkin ◽

D. M. Durand ◽

M. A. Haxhiu

Keyword(s):

Synaptic Transmission ◽

Long Term Potentiation ◽

Rat Hippocampus ◽

Magnesium Concentration ◽

High Frequency Stimulation ◽

Excitatory Postsynaptic Potential ◽

Synaptic Specificity ◽

Term Potentiation ◽

Neuronal Processing

Lyubkin, M., D. M. Durand, and M. A. Haxhiu. Interaction between tetanus long-term potentiation and hypoxia-induced potentiation in the rat hippocampus. J. Neurophysiol. 78: 2475–2482, 1997. The interaction between tetanus-induced long-term potentiation (LTP) and hypoxia-induced potentiation was investigated by performing extracellular recordings in the CA1 region of rat hippocampus using a two-pathway design. Hippocampal slices were placed in an interface chamber containing artificial cerebrospinal fluid (ACSF) solution with high magnesium concentration. Hypoxia was induced by replacing the 5% CO2-95% O2 gas mixture with 5% CO2-95% N2 for 2 min. Tetanus-LTP was induced with 1-s, 100-Hz current pulses. Significant hypoxia-induced potentiation of the slope of the dendritic excitatory postsynaptic potential (EPSP) was found in ACSF containing 2 mM of magnesium 2, 27 ± 10% (mean ± SE; n = 16; P < 0.01) with no change in the mean amplitude of the presynaptic volley. All experiments in which a stable control baseline was obtained were used for data analysis. The data show that short episodes (2 min) of hypoxia can induce LTP of the α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-mediated synaptic transmission. The present study demonstrated that after tetanus-LTP, 33 ± 3% ( n = 10; P < 0.01), hypoxia further potentiated the field EPSP slopes by a mean value of 16 ± 5% ( n = 10; P < 0.05). Moreover, using a two-pathway design, we showed that hypoxia produced similar potentiation in both the control [19 ± 5%; n = 10; P < 0.01) and tetanus-induced LTP pathway, and the total potentiation produced by a combination of tetanus then hypoxia, 63 ± 13% ( n = 10; p < 0.01), was significantly larger ( P < 0.01) than hypoxia alone. These data suggest that hypoxia-induced potentiation is additive with tetanus-LTP. Occlusion experiments were performed to verify whether the mechanisms responsible for hypoxia-induced potentiation are independent of preexisting synaptic levels induced by high-frequency stimulation. Hypoxia produced significant potentiation (23 ± 7%; n = 7; P < 0.05) after successful occlusion of the LTP pathway. Therefore, because the magnitude of hypoxia-induced potentiation is both independent of preexisting synaptic levels and also additive, synaptic specificity associated with LTP is preserved. The magnitude of tetanus-LTP induced 20 min after hypoxia (15 ± 4%; n = 10) was significantly smaller ( P < 0.01) relative to LTP after normoxic conditions (33 ± 3%; n = 10). Additionally, hypoxia blocked the transient, robust potentiation occurring during the early phase of LTP induction. This study suggests that although hypoxia modifies neuronal processing by general excitation, synaptic specificity associated with tetanus-LTP still is preserved. However, hypoxia can disrupt neuronal processing by inhibiting new modification of synaptic transmission.

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Contextual Conditioned Fear Blocks the Induction But Not the Maintenance of Lateral Septal LTP in Behaving Mice

Journal of Neurophysiology ◽

10.1152/jn.1997.78.1.76 ◽

1997 ◽

Vol 78 (1) ◽

pp. 76-81 ◽

Cited By ~ 18

Author(s):

René Garcia ◽

Rose Marie Vouimba ◽

Robert Jaffard

Keyword(s):

Fear Conditioning ◽

Conditioned Fear ◽

Field Potential ◽

Long Term Potentiation ◽

Contextual Fear Conditioning ◽

Lateral Septum ◽

High Frequency Stimulation ◽

Conditioning Chamber ◽

Contextual Fear ◽

Frequency Stimulation

Garcia, René, Rose Marie Vouimba, and Robert Jaffard. Contextual conditioned fear blocks the induction but not the maintenance of lateral septal LTP in behaving mice. J. Neurophysiol. 78: 76–81, 1997. High-frequency stimulation (HFS) of the fimbria induces long-term potentiation (LTP) in the lateral septum. This study was aimed at investigating the effect of contextual fear conditioning on septal LTP with the use of behaving C57 BL/6 mice as subjects. For the acquisition of contextual fear conditioning, animals were placed in a conditioning chamber, where they were subjected to footshocks (FSs, 0.6 mA); the following day (retention), animals were reexposed to the chamber. Animals from the first group received HFS in their home cages before being submitted to conditioning; animals from the second group were first submitted to conditioning before receiving HFS during reexposure to the conditioning chamber; animals from the third group were submitted to the same regimen as those from the second group, except that no FS was delivered in the conditioning chamber; and animals from the fourth group received FS in the conditioning chamber but were maintained in their home cages the day after for LTP induction. Before conditioning, animals from the first group, placed in a familiar context (home cage), displayed an LTP of the N3 wave of septal field potential. After conditioning, reexposure of these animals to the conditioning chamber produced a transient decrease in the amplitude of N3 but did not interfere with the duration of maintenance of LTP. Conversely, in animals from the second group, when HFS was applied during reexposure to the conditioning chamber the induction of LTP was totally blocked. However, mice from the two other groups (3rd and 4th) displayed normal levels of LTP. Taken together with previous findings, these data suggest that contextual conditioned fear may interfere with certain forms of learning via blockade of hippocampal-septal LTP.

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In vivo beta and gamma subthreshold oscillations in rat mitral cells: origin and gating by respiratory dynamics

Journal of Neurophysiology ◽

10.1152/jn.00053.2017 ◽

2018 ◽

Vol 119 (1) ◽

pp. 274-289 ◽

Cited By ~ 1

Author(s):

Nicolas Fourcaud-Trocmé ◽

Virginie Briffaud ◽

Marc Thévenet ◽

Nathalie Buonviso ◽

Corine Amat

Keyword(s):

Membrane Potential ◽

Olfactory Bulb ◽

Local Field ◽

Local Field Potential ◽

Respiratory Rhythm ◽

Field Potential ◽

Synaptic Activity ◽

Spike Discharge ◽

Subthreshold Oscillations

In mammals, olfactory bulb (OB) dynamics are paced by slow and fast oscillatory rhythms at multiple levels: local field potential, spike discharge, and/or membrane potential oscillations. Interactions between these levels have been well studied for the slow rhythm linked to animal respiration. However, less is known regarding rhythms in the fast beta (10–35 Hz) and gamma (35–100 Hz) frequency ranges, particularly at the membrane potential level. Using a combination of intracellular and extracellular recordings in the OB of freely breathing rats, we show that beta and gamma subthreshold oscillations (STOs) coexist intracellularly and are related to extracellular local field potential (LFP) oscillations in the same frequency range. However, they are differentially affected by changes in cell excitability and by odor stimulation. This leads us to suggest that beta and gamma STOs may rely on distinct mechanisms: gamma STOs would mainly depend on mitral cell intrinsic resonance, while beta STOs could be mainly driven by synaptic activity. In a second study, we find that STO occurrence and timing are constrained by the influence of the slow respiratory rhythm on mitral and tufted cells. First, respiratory-driven excitation seems to favor gamma STOs, while respiratory-driven inhibition favors beta STOs. Second, the respiratory rhythm is needed at the subthreshold level to lock gamma and beta STOs in similar phases as their LFP counterparts and to favor the correlation between STO frequency and spike discharge. Overall, this study helps us to understand how the interaction between slow and fast rhythms at all levels of OB dynamics shapes its functional output. NEW & NOTEWORTHY In the mammalian olfactory bulb of a freely breathing anesthetized rat, we show that both beta and gamma membrane potential fast oscillation ranges exist in the same mitral and tufted (M/T) cell. Importantly, our results suggest they have different origins and that their interaction with the slow subthreshold oscillation (respiratory rhythm) is a key mechanism to organize their dynamics, favoring their functional implication in olfactory bulb information processing.

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