Amplification of Odor-Induced Ca<sup>2+</sup> Transients by Store-Operated Ca<sup>2+</sup> Release and Its Role in Olfactory Signal Transduction

Zufall, Frank; Leinders‐Zufall, Trese; Greer, Charles A.

doi:10.1152/jn.2000.83.1.501

Cited by 75 publications

(44 citation statements)

References 64 publications

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“…That SST 3 activation is required for full stimulation of AC by forskolin, a direct activator of AC, suggests the receptor may be acting upstream of ACIII, perhaps blocking an inhibitory constraint such as CaM kinase II, a well established inhibitor of ACIII (Wei et al, 1996). Alternatively, activation of ACIII could generate a Ca 2ϩ transient that is transmitted to and amplified in the neuronal soma, as in olfactory cilia (Zufall et al, 2000). This could activate Ca 2ϩ -dependent ACs such as ACI and ACVIII, leading to a secondary wave of cAMP.…”

Section: Discussionmentioning

confidence: 99%

Somatostatin Signaling in Neuronal Cilia Is Criticalfor Object Recognition Memory

Einstein¹,

Patterson²,

Hon³

et al. 2010

J. Neurosci.

107

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Most neurons possess a single, nonmotile cilium that projects out from the cell surface. These microtubule-based organelles are important in brain development and neurogenesis; however, their function in mature neurons is unknown. Cilia express a complement of proteins distinct from other neuronal compartments, one of which is the somatostatin receptor subtype SST 3 . We show here that SST 3 is critical for object recognition memory in mice. sst3 knock-out mice are severely impaired in discriminating novel objects, whereas they retain normal memory for object location. Further, systemic injection of an SST 3 antagonist (ACQ090) disrupts recall of familiar objects in wild-type mice. To examine mechanisms of SST 3 , we tested synaptic plasticity in CA1 hippocampus. Electrically evoked long-term potentiation (LTP) was normal in sst3 knock-out mice, while adenylyl cyclase/cAMP-mediated LTP was impaired. The SST 3 antagonist also disrupted cAMP-mediated LTP. Basal cAMP levels in hippocampal lysate were reduced in sst3 knock-out mice compared with wild-type mice, while the forskolin-induced increase in cAMP levels was normal. The SST 3 antagonist inhibited forskolin-stimulated cAMP increases, whereas the SST 3 agonist L-796,778 increased basal cAMP levels in hippocampal slices but not hippocampal lysate. Our results show that somatostatin signaling in neuronal cilia is critical for recognition memory and suggest that the cAMP pathway is a conserved signaling motif in cilia. Neuronal cilia therefore represent a novel nonsynaptic compartment crucial for signaling involved in a specific form of synaptic plasticity and in novelty detection.

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Section: Discussionmentioning

confidence: 99%

Somatostatin Signaling in Neuronal Cilia Is Criticalfor Object Recognition Memory

Einstein¹,

Patterson²,

Hon³

et al. 2010

J. Neurosci.

107

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“…Intracellular calcium levels can also increase over larger spatial and temporal scales. This amplification, often through release from intracellular stores (Jaffe and Brown, 1994;Nishiyama et al, 2000;Zufall et al, 2000), can affect cellular processes such as gene expression (West et al, 2001; W. G. that contribute to more persistent synaptic plasticity (Chen W. G. et al, 2003). Thus, it is of interest to visualize intracellular calcium dynamics within a neuron while it undergoes induction and expression of synaptic plasticity.…”

Section: Introductionmentioning

confidence: 99%

The Kinetic Profile of Intracellular Calcium Predicts Long-Term Potentiation and Long-Term Depression

Ismailov¹,

Kalikulov²,

Inoue³

et al. 2004

J. Neurosci.

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Efficiency of synaptic transmission within the neocortex is regulated throughout life by experience and activity. Periods of correlated or uncorrelated presynaptic and postsynaptic activity lead to enduring changes in synaptic efficiency [long-term potentiation (LTP) and long-term depression (LTD), respectively]. The initial plasticity triggering event is thought to be a precipitous rise in postsynaptic intracellular calcium, with higher levels inducing LTP and more moderate levels inducing LTD. We used a pairing protocol in visual cortical brain slices from young guinea pigs with whole-cell recording and calcium imaging to compare the kinetic profiles of calcium signals generated in response to individual pairings along with the cumulative calcium wave and plasticity outcome. The identical pairing protocol applied to layer 2/3 pyramidal neurons results in different plasticity outcomes between cells. These differences are not attributable to variations in the conditioning protocol, cellular properties, inter-animal variability, animal age, differences in spike timing between the synaptic response and spikes, washout of plasticity factors, recruitment of inhibition, or activation of different afferents. The different plasticity outcomes are reliably predicted by individual intracellular calcium transients in the dendrites after the first few pairings. In addition to the differences in the individual calcium transients, the cumulative calcium wave that spreads to the soma also has a different profile for cells that undergo LTP versus LTD. We conclude that there are biological differences between like-type cells in the dendritic calcium signals generated by coincident synaptic input and spiking that determine the sign of the plasticity response after brief associations.

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“…This Ca 2ϩ influx does not depend either on the reverse operation of the Na ϩ /Ca 2ϩ exchanger (DiPolo and Beauge 1987) because we found that its blockage resulted in an increase in the amplitude and duration of the Ca 2ϩ transients. Thus this exchanger probably participates in restoring basal [Ca 2ϩ ] i as has been reported for other neurons (Fierro et al 1998), including ORNs (Jung et al 1994Noe et al 1997;Reisert and Matthews 1998;Zufall et al 2000). Because we found that both ESS and BK responses seem to depend on IP 3 production, it appears likely that this Ca 2ϩ influx depends on activation of an IP 3 conductance in VN dendritic membranes.…”

Section: Component Of Ess Response Dependent On Ca 2ϩ Influxmentioning

confidence: 54%

“…This result differs from otherwise similar Ca 2ϩ signals associated with chemosensory transduction in mouse VN neurons and in ORNs (Leinders-Zufall et al 1997;Restrepo et al 1990Restrepo et al , 1993Sato et al 1991;Schild et al 1995;Tareilus et al 1995), which are completely suppressed in 0 [Ca 2ϩ ] o . It is interesting to note that Ca 2ϩ release from internal Ca 2ϩ pools also occurs in ORNs, but this mechanism appears to be secondary to an initial Ca 2ϩ influx that is mediated through the opening CNG channels (Leinders-Zufall et al 1998;Zufall et al 2000).…”

Section: Component Of Ess Response Dependent On a Ca 2ϩ Releasementioning

confidence: 99%

Calcium Transients in the Garter Snake Vomeronasal Organ

Cinelli

Wang

Chen

et al. 2002

Journal of Neurophysiology

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The signaling cascade involved in chemosensory transduction in the VN organ is incompletely understood. In snakes, the response to nonvolatile prey chemicals is mediated by the vomeronasal (VN) system. Using optical techniques and fluorescent Ca2+ indicators, we found that prey-derived chemoattractants produce initially a transient cytosolic accumulation of [Ca2+]i in the dendritic regions of VN neurons via two pathways: Ca2+release from IP3-sensitive intracellular stores and, to a lesser extent, Ca2+ influx through the plasma membrane. Both components seem to be dependent on IP3 production. Chemoattractants evoke a short-latency Ca2+ elevation even in the absence of extracellular Ca2+, suggesting that in snake VN neurons, Ca2+ release from intracellular stores is independent of a preceding Ca2+ influx, and both components are activated in parallel during early stages of chemosensory transduction. Once the response develops in apical dendritic segments, other mechanisms can also contribute to the amplification and modulation of these chemoattractant-mediated cytosolic Ca2+ transients. In regions close to the cell bodies of the VN neurons, the activation of voltage-sensitive Ca2+ channels and a Ca2+-induced Ca2+ release from intracellular ryanodine-sensitive stores secondarily boost initial cytosolic Ca2+ elevations increasing their magnitude and durations. Return of intracellular Ca2+ to prestimulation levels appears to involve a Ca2+ extrusion mediated by a Na+/Ca2+ exchanger mechanism that probably plays an important role in limiting the magnitude and duration of the stimulation-induced Ca2+ transients.

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Amplification of Odor-Induced Ca²⁺ Transients by Store-Operated Ca²⁺ Release and Its Role in Olfactory Signal Transduction

Cited by 75 publications

References 64 publications

Somatostatin Signaling in Neuronal Cilia Is Criticalfor Object Recognition Memory

Somatostatin Signaling in Neuronal Cilia Is Criticalfor Object Recognition Memory

The Kinetic Profile of Intracellular Calcium Predicts Long-Term Potentiation and Long-Term Depression

Calcium Transients in the Garter Snake Vomeronasal Organ

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Amplification of Odor-Induced Ca2+ Transients by Store-Operated Ca2+ Release and Its Role in Olfactory Signal Transduction

Cited by 75 publications

References 64 publications

Somatostatin Signaling in Neuronal Cilia Is Criticalfor Object Recognition Memory

Somatostatin Signaling in Neuronal Cilia Is Criticalfor Object Recognition Memory

The Kinetic Profile of Intracellular Calcium Predicts Long-Term Potentiation and Long-Term Depression

Calcium Transients in the Garter Snake Vomeronasal Organ

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Product

Resources

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Amplification of Odor-Induced Ca²⁺ Transients by Store-Operated Ca²⁺ Release and Its Role in Olfactory Signal Transduction