Odor-Evoked Oxygen Consumption by Action Potential and Synaptic Transmission in the Olfactory Bulb

Lecoq, Jérôme; Tiret, Pascale; Najac, Marion; Shepherd, Gordon M.; Greer, Charles A.; Charpak, Serge

doi:10.1523/jneurosci.4817-08.2009

Cited by 71 publications

(72 citation statements)

References 51 publications

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“…Thus, the time course of the decrease in CMRO 2 responses followed the decrease in fEPSCs, but not that of the PC cytosolic Ca 2ϩ responses (Fig. 6 E; Table 2), which is consistent with the notion that neurometabolic coupling in cerebral and cerebellar cortex primarily reflects synaptic rather than spiking activity (Viswanathan and Freeman, 2007;Lecoq et al, 2009;Thomsen et al, 2009). CMRO 2 responses also decreased together with decreases in spontaneous and evoked PC spiking (Fig.…”

Section: E;supporting

confidence: 83%

Activity-dependent Increases in Local Oxygen Consumption Correlate with Postsynaptic Currents in the Mouse CerebellumIn Vivo

Mathiesen¹,

Caesar²,

Thomsen³

et al. 2011

J. Neurosci.

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Evoked neural activity correlates strongly with rises in cerebral metabolic rate of oxygen (CMRO 2 ) and cerebral blood flow (CBF). Activity-dependent rises in CMRO 2 fluctuate with ATP turnover due to ion pumping. In vitro studies suggest that increases in cytosolic Ca 2ϩ stimulate oxidative metabolism via mitochondrial signaling, but whether this also occurs in the intact brain is unknown. Here we applied a pharmacological approach to dissect the effects of ionic currents and cytosolic Ca 2ϩ rises of neuronal origin on activitydependent rises in CMRO 2 . We used two-photon microscopy and current source density analysis to study real-time Ca 2ϩ dynamics and transmembrane ionic currents in relation to CMRO 2 in the mouse cerebellar cortex in vivo. We report a direct correlation between CMRO 2 and summed (i.e., the sum of excitatory, negative currents during the whole stimulation period) field EPSCs (ΑfEPSCs) in Purkinje cells (PCs) in response to stimulation of the climbing fiber (CF) pathway. Blocking stimulus-evoked rises in cytosolic Ca 2ϩ in PCs with the P/Q-type channel blocker -agatoxin-IVA (-AGA), or the GABA A receptor agonist muscimol, did not lead to a time-locked reduction in CMRO 2 , and excitatory synaptic or action potential currents. During stimulation, neither -AGA or (-oxo)-bis-(transformatotetramine-ruthenium) (Ru360), a mitochondrial Ca 2ϩ uniporter inhibitor, affected the ratio of CMRO 2 to fEPSCs or evoked local field potentials. However, baseline CBF and CMRO 2 decreased gradually with Ru360. Our data suggest that in vivo activity-dependent rises in CMRO 2 are correlated with synaptic currents and postsynaptic spiking in PCs. Our study did not reveal a unique role of neuronal cytosolic Ca 2ϩ signals in controlling CMRO 2 increases during CF stimulation.

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Section: E;supporting

confidence: 83%

Activity-dependent Increases in Local Oxygen Consumption Correlate with Postsynaptic Currents in the Mouse CerebellumIn Vivo

Mathiesen¹,

Caesar²,

Thomsen³

et al. 2011

J. Neurosci.

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“…Measurements of oxygen partial pressure (P tiss,O2 ) were made with Clark-type oxygen microsensors (2-to 5-μm tip diameter) (14,16,(21)(22)(23), which were directly inserted into GH cell clusters in anesthetized GH-eGFP mice ventilated with variable air/O 2 mixtures. Resting P tiss,O2 values were 33.8 ± 1.7 mmHg in the presence of atmospheric air (n = 4), and increased up to 57.3 ± 5.5 mmHg in a mixture of 50% atmospheric air/50% O 2 (n = 15; Fig.…”

Section: Resultsmentioning

confidence: 99%

“…To measure velocities of RBCs in individual capillaries, injections were made via the jugular vein catheter of solutions of dextrans of different molecular weights (from 4.4 to 500 kDa) linked to different colored fluorescent probes: Cascade Blue, FITC, rhodamine, and Texas Red (Molecular Probes and Sigma-Aldrich). To measure partial oxygen pressure (P tiss,O2 ), recordings were made with Clark-type polarographic oxygen microsensors (Unisense) polarized at −0.8 V, as previously reported (23). Fluorescent dextrans were introduced by iontophoresis from a glass micropipette.…”

Section: Methodsmentioning

confidence: 99%

Cellular in vivo imaging reveals coordinated regulation of pituitary microcirculation and GH cell network function

Lafont

Desarménien

Cassou

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Growth hormone (GH) exerts its actions via coordinated pulsatile secretion from a GH cell network into the bloodstream. Practically nothing is known about how the network receives its inputs in vivo and releases hormones into pituitary capillaries to shape GH pulses. Here we have developed in vivo approaches to measure local blood flow, oxygen partial pressure, and cell activity at single-cell resolution in mouse pituitary glands in situ. When secretagogue (GHRH) distribution was modeled with fluorescent markers injected into either the bloodstream or the nearby intercapillary space, a restricted distribution gradient evolved within the pituitary parenchyma. Injection of GHRH led to stimulation of both GH cell network activities and GH secretion, which was temporally associated with increases in blood flow rates and oxygen supply by capillaries, as well as oxygen consumption. Moreover, we observed a time-limiting step for hormone output at the perivascular level; macromolecules injected into the extracellular parenchyma moved rapidly to the perivascular space, but were then cleared more slowly in a size-dependent manner into capillary blood. Our findings suggest that GH pulse generation is not simply a GH cell network response, but is shaped by a tissue microenvironment context involving a functional association between the GH cell network activity and fluid microcirculation.blood flow | hormone pulsatility | oxygen pressure | tissue microenvironment | extracellular space

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“…2008; Coutinho et al 2004;Lecoq et al 2009;Offenhauser et al 2005;Reinert et al 2004;Sinha et al 1999Sinha et al , 2004.…”

Section: Postsynaptic Excitation and Cmro 2 During Parallel Fiber Stiunclassified

“…Both postsynaptic excitation and action potentials perturb the ionic balance of Na ϩ , K ϩ , and Ca 2ϩ ions across the cell membrane (Ames 3rd 2000; Attwell and Laughlin 2001;Erecinska and Silver 1989;Lennie 2003), requiring energy and thus glucose and oxygen to restore it. Findings from primates (Rauch et al 2008), felines (Viswanathan and Freeman 2007), and rats (Caesar et al 2003;Lecoq et al 2009;Offenhauser et al 2005) all indicate that postsynaptic excitation is a major consumer of cortical oxygen. Evidence supporting this comes from cytochrome oxidase histochemical studies.…”

Section: Introductionmentioning

confidence: 99%

Principal Cell Spiking, Postsynaptic Excitation, and Oxygen Consumption in the Rat Cerebellar Cortex

Thomsen

Piilgaard

Gjedde³

et al. 2009

Journal of Neurophysiology

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Thomsen K, Piilgaard H, Gjedde A, Bonvento G, Lauritzen M. Principal cell spiking, postsynaptic excitation, and oxygen consumption in the rat cerebellar cortex. J Neurophysiol 102: 1503-1512, 2009. First published July 1, 2009 doi:10.1152/jn.00289.2009. One contention within the field of neuroimaging concerns the character of the depicted activity: Does it represent neuronal action potential generation (i.e., spiking) or postsynaptic excitation? This question is related to the metabolic costs of different aspects of neurosignaling. The cerebellar cortex is well suited for addressing this problem because synaptic input to and spiking of the principal cell, the Purkinje cell (PC), are spatially segregated. Also, PCs are pacemakers, able to generate spikes endogenously. We examined the contributions to cerebellar cortical oxygen consumption (CMRO 2 ) of postsynaptic excitation and PC spiking during evoked and ongoing neuronal activity in the rat. By inhibiting excitatory synaptic input using ionotropic glutamate receptor blockers, we found that the increase in CMRO 2 evoked by parallel fiber (PF) stimulation depended entirely on postsynaptic excitation. In contrast, PC spiking was largely responsible for the increase in CMRO 2 when ongoing neuronal activity was increased by ␥-aminobutyric acid type A receptor blockade. In this case, CMRO 2 increased equally during PC spiking with excitatory synaptic activity as during PC pacemaker spiking without excitatory synaptic input. Subsequent inhibition of action potential propagation and neurotransmission by blocking voltage-gated Na ϩ -channels eliminated the increases in CMRO 2 due to PF stimulation and increased PC spiking, but left a large fraction of CMRO 2 , i.e., basal CMRO 2 , intact. In conclusion, whereas basal CMRO 2 in anesthetized animals did not seem to be related to neurosignaling, increases in CMRO 2 could be induced by all aspects of neurosignaling. Our findings imply that CMRO 2 responses cannot a priori be assigned to specific neuronal activities.

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Odor-Evoked Oxygen Consumption by Action Potential and Synaptic Transmission in the Olfactory Bulb

Cited by 71 publications

References 51 publications

Activity-dependent Increases in Local Oxygen Consumption Correlate with Postsynaptic Currents in the Mouse CerebellumIn Vivo

Activity-dependent Increases in Local Oxygen Consumption Correlate with Postsynaptic Currents in the Mouse CerebellumIn Vivo

Cellular in vivo imaging reveals coordinated regulation of pituitary microcirculation and GH cell network function

Principal Cell Spiking, Postsynaptic Excitation, and Oxygen Consumption in the Rat Cerebellar Cortex

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