Selective Enhancement of P-Type Calcium Currents by Isoproterenol in the Rat Amygdala

We investigated activation of β-adrenergic receptor–adenylyl cyclase–cAMP cascade on the whole-cell voltage-dependent Ca2+ currents (ICa) in acutely isolated rat basolateral amygdala neurons. Application of β-receptor agonist isoproterenol (Iso) caused a long-term enhancement ofICa. The effect of Iso was blocked by concurrent application of β-receptor antagonist propranolol. However, delayed application of propranolol after theICa enhancement did not affect Iso-induced potentiation, suggesting that the sustained effect was not caused by a slow washout of Iso. Nimodipine and ω-conotoxin-GVIA reduced theICa by ∼35 and ∼29%, respectively, without reducing enhancement of ICa by Iso significantly. The modulation appeared to involve P-type current, because the enhancement was abolished after pretreatment with ω-agatoxin-IVA. Forskolin, an adenylyl cyclase activator, mimicked the action of Iso in enhancing ICa, and this effect was blocked by an inhibitor of cAMP cascade, indicating a cAMP-dependent mechanism. Iso also induced a long-term potentiation (LTP) of synaptic transmission, which could be prevented by P-type Ca2+ channel blockers. These results suggest that P-type Ca2+ channels were selectively upregulated in the basolateral amygdala neurons, and enhancement of P-type currents could contribute to presynaptic form of LTP.

[1]  E. Kavalali,et al.  cAMP-Dependent Enhancement of Dihydropyridine-Sensitive Calcium Channel Availability in Hippocampal Neurons , 1997, The Journal of Neuroscience.

[2]  K. Hsu,et al.  Inhibition of N‐type calcium currents by lamotrigine in rat amygdalar neurones , 1996, Neuroreport.

[3]  A. Akaike,et al.  Cyclic AMP-dependent modulation of N- and Q-type Ca2+ channels expressed in Xenopus oocytes , 1996, Neuroscience Letters.

[4]  P. Haydon,et al.  Direct Modulation of the Secretory Machinery Underlies PKA-Dependent Synaptic Facilitation in Hippocampal Neurons , 1996, Neuron.

[5]  B. Hille,et al.  Modulation of High Voltage-Activated Calcium Channels by Somatostatin in Acutely Isolated Rat Amygdaloid Neurons , 1996, The Journal of Neuroscience.

[6]  Mark J. Thomas,et al.  Activity-Dependent β-Adrenergic Modulation of Low Frequency Stimulation Induced LTP in the Hippocampal CA1 Region , 1996, Neuron.

[7]  Paul Antoine Salin,et al.  Cyclic AMP Mediates a Presynaptic Form of LTP at Cerebellar Parallel Fiber Synapses , 1996, Neuron.

[8]  P W Gean,et al.  Isoproterenol potentiates synaptic transmission primarily by enhancing presynaptic calcium influx via P- and/or Q-type calcium channels in the rat amygdala , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  A. Dolphin.  Facilitation of Ca2+ current in excitable cells , 1996, Trends in Neurosciences.

[10]  E R Kandel,et al.  Presynaptic facilitation revisited: state and time dependence , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  R. Iyengar,et al.  Postsynaptic CAMP pathway gates early LTP in hippocampal CA1 region , 1995, Neuron.

[12]  James L. McGaugh,et al.  The amygdala and emotional memory , 1995, Nature.

[13]  G. Fain,et al.  Neurotransmitter receptors of starburst amacrine cells in rabbit retinal slices , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  R. Tsien,et al.  Pharmacological dissection of multiple types of Ca2+ channel currents in rat cerebellar granule neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  James L. McGaugh,et al.  β-Adrenergic activation and memory for emotional events , 1994, Nature.

[16]  E. Kandel,et al.  cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase , 1994, Cell.

[17]  R. Nicoll,et al.  Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. , 1994, Science.

[18]  P. Conn,et al.  Presynaptic enhancement of excitatory synaptic transmission by beta-adrenergic receptor activation. , 1994, Journal of neurophysiology.

[19]  B. Gustafsson,et al.  TEA elicits two distinct potentiations of synaptic transmission in the CA1 region of the hippocampal slice , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  R. Tsien,et al.  Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. , 1994, Science.

[21]  A. Momiyama,et al.  Different types of calcium channels mediate central synaptic transmission , 1993, Nature.

[22]  J. Luebke,et al.  Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus , 1993, Neuron.

[23]  Yy Huang,et al.  Examination of TEA-induced synaptic enhancement in area CA1 of the hippocampus: the role of voltage-dependent Ca2+ channels in the induction of LTP , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  M. Adams,et al.  Differential activation of adenosine receptors decreases N-type but potentiates P-type Ca2+ current in hippocampal CA3 neurons , 1993, Neuron.

[25]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[26]  H. C. Moises,et al.  Inhibitory responses of rat basolateral amygdaloid neurons recorded in vitro , 1992, Neuroscience.

[27]  Charles F. Stevens,et al.  Modulation of synaptic efficacy in field CA1 of the rat hippocampus by forskolin , 1992, Brain Research.

[28]  M. Adams,et al.  P-type calcium channels blocked by the spider toxin ω-Aga-IVA , 1992, Nature.

[29]  E. Asprodini,et al.  Excitatory transmission in the basolateral amygdala. , 1991, Journal of neurophysiology.

[30]  Y. Ben-Ari,et al.  Novel form of long-term potentiation produced by a K+channel blocker in the hippocampus , 1991, Nature.

[31]  Robert K. S. Wong,et al.  Isolation of neurons suitable for patch-clamping from adult mammalian central nervous systems , 1986, Journal of Neuroscience Methods.

[32]  J. D. McGaugh,et al.  Modulating effects of posttraining epinephrine on memory: Involvement of the amygdala noradrenergic system , 1986, Brain Research.

[33]  R. Llinás,et al.  Presynaptic calcium currents in squid giant synapse. , 1981, Biophysical journal.

[34]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[35]  R. Foehring,et al.  Multiple high-threshold calcium currents in acutely isolated rat amygdaloid pyramidal cells. , 1994, Journal of neurophysiology.

[36]  J. D. McGaugh,et al.  Beta-adrenergic activation and memory for emotional events. , 1994, Nature.

[37]  E. Asprodini,et al.  Inhibitory transmission in the basolateral amygdala. , 1991, Journal of neurophysiology.

[38]  Daniel Johnston,et al.  Noradrenaline and β-adrenoceptor agonists increase activity of voltage-dependent calcium channels in hippocampal neurons , 1987, Nature.

[39]  P. Greengard,et al.  Protein phosphorylation in the nervous system , 1984 .