Postsynaptic Induction and PKA-Dependent Expression of LTP in the Lateral Amygdala

Whereas much is now known about the behavioral importance of the lateral nucleus of the amygdala for the storage of implicit memories of fear, little is known in molecular terms about the signal transduction pathways required for long-term potentiation (LTP) in this nucleus. Using brain slices containing the amygdala, we have studied LTP in the pathway from external capsule to the lateral nucleus, a pathway that mediates information from the auditory cortex important for fear conditioning. We found the induction of LTP is postsynaptic; it is dependent on postsynaptic depolarization, on the influx of Ca2+ into the postsynaptic cell and, at least in part, on the activation of N-methyl-D-aspartate (NMDA) receptors. The LTP is associated with a decrease of paired-pulse facilitation (PPF) and is blocked by bath application but not blocked by postsynaptic injection of inhibitors of the cyclic adenosine monophosphate-dependent (cAMP-dependent) protein kinase (PKA). Consistent with the possibility that the expression might involve PKA presynaptically, the adenylyl cyclase activator forskolin induced synaptic potentiation of this pathway that also was associated with a decrease of PPF, and this potentiation occluded the tetanus-induced LTP.

[1]  D. Johnston,et al.  Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  R. Zucker.  Changes in the statistics of transmitter release during facilitation , 1973, The Journal of physiology.

[3]  R. Nicoll,et al.  Comparison of two forms of long-term potentiation in single hippocampal neurons. , 1990, Science.

[4]  A. McDonald.  Neurons of the lateral and basolateral amygdaloid nuclei: A golgi study in the rat , 1982, The Journal of comparative neurology.

[5]  Y. Ikegaya,et al.  Roles of GABAA, NMDA and muscarinic receptors in induction of long-term potentiation in the medial and lateral amygdala in vitro , 1995, Neuroscience Research.

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

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

[8]  R. Nicoll,et al.  Mechanisms underlying potentiation of synaptic transmission in rat anterior cingulate cortex in vitro. , 1991, The Journal of physiology.

[9]  Daly Jw,et al.  Forskolin: its biological and chemical properties. , 1986, Advances in cyclic nucleotide and protein phosphorylation research.

[10]  Joseph E LeDoux.  Emotion: clues from the brain. , 1995, Annual review of psychology.

[11]  P. Schulz,et al.  Long-term potentiation involves increases in the probability of neurotransmitter release. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[12]  U. Kuhnt,et al.  Interaction between paired-pulse facilitation and long-term potentiation in area ca1 of guinea-pig hippocampal slices: Application of quantal analysis , 1994, Neuroscience.

[13]  B. Sakmann,et al.  Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices. , 1992, The Journal of physiology.

[14]  E. Kandel,et al.  Modulation of Both the Early and the Late Phase of Mossy Fiber LTP by the Activation of β-Adrenergic Receptors , 1996, Neuron.

[15]  B. Gustafsson,et al.  Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  E. Kandel,et al.  Genetic Demonstration of a Role for PKA in the Late Phase of LTP and in Hippocampus-Based Long-Term Memory , 1997, Cell.

[17]  Joseph E LeDoux,et al.  Fear conditioning induces associative long-term potentiation in the amygdala , 1997, Nature.

[18]  E. W. Kairiss,et al.  Long‐Term synaptic potentiation in the amygdala , 1990, Synapse.

[19]  A. Chiba,et al.  The amygdala and emotion , 1996, Current Opinion in Neurobiology.

[20]  D. Dixon,et al.  Adenylate cyclase system is essential for long-term facilitation at the crayfish neuromuscular junction , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  P. Chapman,et al.  Induction of long‐term potentiation in the basolateral amygdala does not depend on NMDA receptor activation , 1992, Synapse.

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

[23]  E. Kandel,et al.  Control of Memory Formation Through Regulated Expression of a CaMKII Transgene , 1996, Science.

[24]  Gary Lynch,et al.  Response to repetitive stimulation of AMPA receptors in patches excised from fields CA1 and CA3 of the hippocampus , 1996, Brain Research.

[25]  H. Wigström,et al.  Phorbol ester-induced synaptic potentiation differs from long-term potentiation in the guinea pig hippocampus in vitro , 1988, Neuroscience Letters.

[26]  Y. Dudai,et al.  cAMP Response Element-Binding Protein in the Amygdala Is Required for Long- but not Short-Term Conditioned Taste Aversion Memory , 1997, The Journal of Neuroscience.

[27]  P. Kelly,et al.  Regulation of synaptic facilitation by postsynaptic Ca2+/CaM pathways in hippocampal CA1 neurons. , 1996, Journal of neurophysiology.

[28]  R. Nicoll,et al.  Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. , 1993, Journal of neurophysiology.

[29]  E. Kandel,et al.  A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[30]  E. Kandel,et al.  Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. , 1994, Learning & memory.

[31]  Michael Davis,et al.  Neurotransmission in the rat amygdala related to fear and anxiety , 1994, Trends in Neurosciences.

[32]  Joseph E LeDoux,et al.  Convergent but temporally separated inputs to lateral amygdala neurons from the auditory thalamus and auditory cortex use different postsynaptic receptors: in vivo intracellular and extracellular recordings in fear conditioning pathways. , 1996, Learning & memory.

[33]  R. Nicoll,et al.  Contrasting properties of two forms of long-term potentiation in the hippocampus , 1995, Nature.

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

[35]  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.

[36]  Gary Lynch,et al.  Evidence that changes in presynaptic calcium currents are not responsible for long-term potentiation in hippocampus , 1989, Brain Research.

[37]  C. Jahr,et al.  Synaptic transmission between dorsal root ganglion and dorsal horn neurons in culture: antagonism of monosynaptic excitatory postsynaptic potentials and glutamate excitation by kynurenate , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  Gean Po-wu,et al.  Long-term enhancement of EPSP and NMDA receptor-mediated synaptic transmission in the amygdala , 1993, Brain Research Bulletin.

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

[40]  Joseph E. LeDoux,et al.  LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit , 1995, Neuron.

[41]  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.

[42]  B. Gustafsson,et al.  Long-term potentiation and paired-pulse facilitation in the hippocampal CA1 region. , 1996, Neuroreport.

[43]  M. McKERNAN,et al.  Fear conditioning induces a lasting potentiation of synaptic currents in vitro , 1997, Nature.

[44]  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.

[45]  W. Abraham,et al.  Differential regulation of paired-pulse plasticity following LTP in the dentate gyrus. , 1994, Neuroreport.

[46]  M. Fanselow,et al.  The Amygdala and Fear Conditioning: Has the Nut Been Cracked? , 1996, Neuron.

[47]  Joseph E LeDoux.  The emotional brain , 1996 .