Distribution of IP3-mediated calcium responses and their role in nuclear signalling in rat basolateral amygdala neurons.
Metabotropic receptor activation is important for learning, memory and synaptic plasticity in the amygdala and other brain regions. Synaptic stimulation of metabotropic receptors in basolateral amygdala (BLA) projection neurons evokes a focal rise in free Ca(2+) in the dendrites that propagate as waves into the soma and nucleus. These Ca(2+) waves initiate in the proximal dendrites and show limited propagation centrifugally away from the soma. In other cell types, Ca(2+) waves have been shown to be mediated by either metabotropic glutamate receptor (mGluR) or muscarinic receptor (mAChR) activation. Here we show that mGluRs and mAChRs act cooperatively to release Ca(2+) from inositol 1,4,5-trisphosphate (IP(3))-sensitive intracellular Ca(2+) stores. Whereas action potentials (APs) alone were relatively ineffective in raising nuclear Ca(2+), their pairing with metabotropic receptor activation evoked an IP(3)-receptor-mediated Ca(2+)-induced Ca(2+) release, raising nuclear Ca(2+) into the micromolar range. Metabotropic-receptor-mediated Ca(2+)-store release was highly compartmentalized. When coupled with metabotropic receptor stimulation, large robust Ca(2+) rises and AP-induced amplification were observed in the soma, nucleus and sparsely spiny dendritic segments with metabotropic stimulation. In contrast, no significant amplification of the Ca(2+) transient was detected in spine-dense high-order dendritic segments. Ca(2+) rises evoked by photolytic uncaging of IP(3) showed the same distribution, suggesting that IP(3)-sensitive Ca(2+) stores are preferentially located in the soma and proximal dendrites. This distribution of metabotropic-mediated store release suggests that the neuromodulatory role of metabotropic receptor stimulation in BLA-dependent learning may result from enhanced nuclear signalling.
Power
John M
JM
Queensland Brain Institute, The University of Queensland, St Lucia, Queensland 4072, Australia.
Sah
Pankaj
P
D000200:Action Potentials / Q000502:physiology; D000679:Amygdala / Q000378:metabolism*; D000818:Animals; D002118:Calcium / Q000378:metabolism*; D002467:Cell Nucleus / Q000378:metabolism*; D003712:Dendrites / Q000378:metabolism; D066298:In Vitro Techniques; D015544:Inositol 1,4,5-Trisphosphate / Q000502:physiology*; D009474:Neurons / Q000378:metabolism*; D051381:Rats; D017208:Rats, Wistar; D018094:Receptors, Metabotropic Glutamate / Q000378:metabolism; D011976:Receptors, Muscarinic / Q000378:metabolism; D015398:Signal Transduction / Q000502:physiology*; D014018:Tissue Distribution
D018094:Receptors, Metabotropic Glutamate; D011976:Receptors, Muscarinic; D015544:Inositol 1,4,5-Trisphosphate; D002118:Calcium