Priming of intracellular calcium stores in rat CA1 pyramidal neurons

Repetitive synaptic stimulation evokes large amplitude Ca2+ release waves from internal stores in many kinds of pyramidal neurons. The waves result from mGluR mobilization of IP3 leading to Ca2+‐induced Ca2+ release. In most experiments in slices, regenerative Ca2+ release can be evoked for only a few trials. We examined the conditions required for consistent release from the internal stores in hippocampal CA1 pyramidal neurons. We found that priming with action potentials evoked at 0.5–1 Hz for intervals as short as 15 s were sufficient to fill the stores, while sustained subthreshold depolarization or subthreshold synaptic stimulation lasting from 15 s to 2 min was less effective. A single episode of priming was effective for about 2–3 min. Ca2+ waves could also be evoked by uncaging IP3 with a UV flash in the dendrites. Priming was necessary to evoke these waves repetitively; 7–10 spikes in 15 s were again effective for this protocol, indicating that priming acts to refill the stores and not at a site upstream to the production of IP3. These results suggest that normal spiking activity of pyramidal neurons in vivo should be sufficient to maintain their internal stores in a primed state ready to release Ca2+ in response to an appropriate physiological stimulus. This may be a novel form of synaptic plasticity where a cell's capacity to release Ca2+ is modulated by its average firing frequency.

[1]  Y. E. Goldman,et al.  Kinetics of smooth and skeletal muscle activation by laser pulse photolysis of caged inositol 1,4,5-trisphosphate , 1987, Nature.

[2]  M. Iino,et al.  Biphasic Ca2+ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth muscle cells of the guinea pig taenia caeci , 1990, The Journal of general physiology.

[3]  James Watras,et al.  Bell-shaped calcium-response curves of lns(l,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum , 1991, Nature.

[4]  R. Huganir,et al.  Inositol 1,4,5-trisphosphate receptor is phosphorylated by cyclic AMP-dependent protein kinase at serines 1755 and 1589. , 1991, Biochemical and biophysical research communications.

[5]  S. M. Goldin,et al.  Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. , 1991, Science.

[6]  W. N. Ross,et al.  High time resolution fluorescence imaging with a CCD camera , 1991, Journal of Neuroscience Methods.

[7]  S. Rhee,et al.  Regulation of inositol phospholipid-specific phospholipase C isozymes. , 1992, The Journal of biological chemistry.

[8]  K.,et al.  Cyclic AMP-dependent phosphorylation of an immunoaffinity-purified homotetrameric inositol 1,4,5-trisphosphate receptor (type I) increases Ca2+ flux in reconstituted lipid vesicles. , 1994, The Journal of biological chemistry.

[9]  T. H. Brown,et al.  Metabotropic glutamate receptor activation induces calcium waves within hippocampal dendrites. , 1994, Journal of neurophysiology.

[10]  B. Sakmann,et al.  Patch-Pipette Recordings from the Soma, Dendrites, and Axon of Neurons in Brain Slices , 1995 .

[11]  D. Johnston,et al.  Subthreshold synaptic activation of voltage-gated Ca2+ channels mediates a localized Ca2+ influx into the dendrites of hippocampal pyramidal neurons. , 1995, Journal of neurophysiology.

[12]  D. Johnston,et al.  Dihydropyridine-sensitive, voltage-gated Ca2+ channels contribute to the resting intracellular Ca2+ concentration of hippocampal CA1 pyramidal neurons. , 1996, Journal of neurophysiology.

[13]  J. Connor,et al.  Ca2+ release from intracellular stores induced by afferent stimulation of CA3 pyramidal neurons in hippocampal slices. , 1996, Journal of neurophysiology.

[14]  B. Sakmann,et al.  Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons. , 1996, Biophysical journal.

[15]  A Konnerth,et al.  Release and sequestration of calcium by ryanodine‐sensitive stores in rat hippocampal neurones , 1997, The Journal of physiology.

[16]  George J. Augustine,et al.  Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites , 1998, Nature.

[17]  C. Fiorillo,et al.  Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons , 1998, Nature.

[18]  W. N. Ross,et al.  Synergistic Release of Ca2+ from IP3-Sensitive Stores Evoked by Synaptic Activation of mGluRs Paired with Backpropagating Action Potentials , 1999, Neuron.

[19]  Daniel Johnston,et al.  Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism , 1999, Nature Neuroscience.

[20]  C. Misquitta,et al.  Sarco/endoplasmic reticulum Ca2+ (SERCA)-pumps: link to heart beats and calcium waves. , 1999, Cell calcium.

[21]  W. N. Ross,et al.  Inositol 1,4,5-Trisphosphate (IP3)-Mediated Ca2+ Release Evoked by Metabotropic Agonists and Backpropagating Action Potentials in Hippocampal CA1 Pyramidal Neurons , 2000, The Journal of Neuroscience.

[22]  D M Bers,et al.  Calcium fluxes involved in control of cardiac myocyte contraction. , 2000, Circulation research.

[23]  J. Csicsvari,et al.  Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[24]  T. Freund,et al.  Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells , 2001, Neuroscience.

[25]  B. Sakmann,et al.  In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain , 2002, Pflügers Archiv.

[26]  W. N. Ross,et al.  Spatial Segregation and Interaction of Calcium Signalling Mechanisms in Rat Hippocampal CA1 Pyramidal Neurons , 2002, The Journal of physiology.

[27]  W. N. Ross,et al.  Threshold conditions for synaptically evoking Ca(2+) waves in hippocampal pyramidal neurons. , 2002, Journal of neurophysiology.

[28]  Pankaj Sah,et al.  Nuclear Calcium Signaling Evoked by Cholinergic Stimulation in Hippocampal CA1 Pyramidal Neurons , 2002, The Journal of Neuroscience.

[29]  Kamran Khodakhah,et al.  Two Intracellular Pathways Mediate Metabotropic Glutamate Receptor-Induced Ca2+ Mobilization in Dopamine Neurons , 2003, The Journal of Neuroscience.

[30]  A. Parekh The Wellcome Prize Lecture , 2003 .

[31]  Shigeo Watanabe,et al.  Synaptically Activated Ca2+ Waves in Layer 2/3 and Layer 5 Rat Neocortical Pyramidal Neurons , 2003, The Journal of physiology.

[32]  A. Parekh Store-operated Ca2+ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane. , 2003, The Journal of physiology.

[33]  Ian Parker,et al.  Ca2+ Signaling in Mouse Cortical Neurons Studied by Two-Photon Imaging and Photoreleased Inositol Triphosphate , 2003, The Journal of Neuroscience.

[34]  Larry E Wagner,et al.  Modulation of cytosolic calcium signaling by protein kinase A-mediated phosphorylation of inositol 1,4,5-trisphosphate receptors. , 2004, Biological research.

[35]  J. Putney,et al.  Capacitative calcium entry , 1997, The Journal of cell biology.

[36]  J. Power,et al.  Intracellular calcium store filling by an L‐type calcium current in the basolateral amygdala at subthreshold membrane potentials , 2005, The Journal of physiology.

[37]  Michael D. Cahalan,et al.  STIM1, an essential and conserved component of store-operated Ca2+ channel function , 2005, The Journal of cell biology.

[38]  Nelson Spruston,et al.  Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites , 2005, The Journal of physiology.

[39]  D. Ogden,et al.  Kinetic, pharmacological and activity‐dependent separation of two Ca2+ signalling pathways mediated by type 1 metabotropic glutamate receptors in rat Purkinje neurones , 2006, The Journal of physiology.

[40]  Shigeo Watanabe,et al.  Modulation of calcium wave propagation in the dendrites and to the soma of rat hippocampal pyramidal neurons , 2006, The Journal of physiology.

[41]  P. Sah,et al.  Distribution of IP3‐mediated calcium responses and their role in nuclear signalling in rat basolateral amygdala neurons , 2007, The Journal of physiology.

[42]  M. Yeckel,et al.  MGluR-mediated calcium waves that invade the soma regulate firing in layer V medial prefrontal cortical pyramidal neurons. , 2008, Cerebral cortex.