Coactivation of Thalamic and Cortical Pathways Induces Input Timing-Dependent Plasticity in Amygdala

Long-term synaptic enhancements in cortical and thalamic auditory inputs to the lateral nucleus of the amygdala (LAn) mediate encoding of conditioned fear memory. It is not known, however, whether the convergent auditory conditioned stimulus (CSa) pathways interact with each other to produce changes in their synaptic function. We found that continuous paired stimulation of thalamic and cortical auditory inputs to the LAn with the interstimulus delay approximately mimicking a temporal pattern of their activation in behaving animals during auditory fear conditioning resulted in persistent potentiation of synaptic transmission in the cortico-amygdala pathway in rat brain slices. This form of input timing–dependent plasticity (ITDP) in cortical input depends on inositol 1,4,5-trisphosphate (InsP3)-sensitive Ca2+ release from internal stores and postsynaptic Ca2+ influx through calcium-permeable kainate receptors during its induction. ITDP in the auditory projections to the LAn, determined by characteristics of presynaptic activity patterns, may contribute to the encoding of the complex CSa.

[1]  M. Mayer,et al.  Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block , 1995, Neuron.

[2]  Joseph E LeDoux,et al.  GABAA and GABAB receptors differentially regulate synaptic transmission in the auditory thalamo‐amygdala pathway: An in vivo microiontophoretic study and a model , 1996, Synapse.

[3]  J. E. Huettner,et al.  Q/R Site Editing Controls Kainate Receptor Inhibition by Membrane Fatty Acids , 2005, The Journal of Neuroscience.

[4]  Joseph E LeDoux,et al.  Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  D. Paré,et al.  Similar inhibitory processes dominate the responses of cat lateral amygdaloid projection neurons to their various afferents. , 1997, Journal of neurophysiology.

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

[7]  M. Zhuo,et al.  Altered Behavioral Responses to Noxious Stimuli and Fear in Glutamate Receptor 5 (GluR5)- or GluR6-Deficient Mice , 2005, The Journal of Neuroscience.

[8]  Joseph E LeDoux,et al.  Stimulus generalization of fear responses: effects of auditory cortex lesions in a computational model and in rats. , 1997, Cerebral cortex.

[9]  Pankaj Sah,et al.  Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala , 1998, Nature.

[10]  B. Sakmann,et al.  Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues. , 1996, The Journal of physiology.

[11]  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.

[12]  E. Kandel,et al.  stathmin, a Gene Enriched in the Amygdala, Controls Both Learned and Innate Fear , 2005, Cell.

[13]  Y. Humeau,et al.  Presynaptic induction of heterosynaptic associative plasticity in the mammalian brain , 2003, Nature.

[14]  E. Tsvetkov,et al.  Glutamate Uptake Determines Pathway Specificity of Long-Term Potentiation in the Neural Circuitry of Fear Conditioning , 2004, Neuron.

[15]  Joseph E LeDoux,et al.  Fear Conditioning Enhances Different Temporal Components of Tone-Evoked Spike Trains in Auditory Cortex and Lateral Amygdala , 1997, Neuron.

[16]  S. Redman,et al.  Different calcium sources are narrowly tuned to the induction of different forms of LTP. , 2002, Journal of neurophysiology.

[17]  R. Shin,et al.  Hierarchical order of coexisting pre- and postsynaptic forms of long-term potentiation at synapses in amygdala , 2010, Neuroscience Research.

[18]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[19]  M. Zhuo,et al.  Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord , 1999, Nature.

[20]  S. Siegelbaum,et al.  A Role for Synaptic Inputs at Distal Dendrites: Instructive Signals for Hippocampal Long-Term Plasticity , 2007, Neuron.

[21]  Karel Svoboda,et al.  Locally dynamic synaptic learning rules in pyramidal neuron dendrites , 2007, Nature.

[22]  E. Tsvetkov,et al.  Spatiotemporal Asymmetry of Associative Synaptic Plasticity in Fear Conditioning Pathways , 2006, Neuron.

[23]  Joseph E LeDoux,et al.  Postsynaptic Receptor Trafficking Underlying a Form of Associative Learning , 2005, Science.

[24]  Joseph E LeDoux,et al.  Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. , 1993, Cerebral cortex.

[25]  Yan Li,et al.  Norepinephrine enables the induction of associative long-term potentiation at thalamo-amygdala synapses , 2007, Proceedings of the National Academy of Sciences.

[26]  Eric R. Kandel,et al.  Fear Conditioning Occludes LTP-Induced Presynaptic Enhancement of Synaptic Transmission in the Cortical Pathway to the Lateral Amygdala , 2002, Neuron.

[27]  Joseph E LeDoux,et al.  Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat , 1985, The Journal of comparative neurology.

[28]  D. Paré,et al.  Neuronal Correlates of Fear in the Lateral Amygdala: Multiple Extracellular Recordings in Conscious Cats , 2000, The Journal of Neuroscience.

[29]  Y. Humeau,et al.  Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition , 2003, Nature Neuroscience.

[30]  Joseph E LeDoux,et al.  Response properties of single units in areas of rat auditory thalamus that project to the amygdala , 1994, Experimental Brain Research.

[31]  R. North,et al.  Membrane properties and synaptic potentials of three types of neurone in rat lateral amygdala. , 1993, The Journal of physiology.

[32]  Joseph E. LeDoux,et al.  A Recurrent Network in the Lateral Amygdala: A Mechanism for Coincidence Detection , 2008, Frontiers in neural circuits.

[33]  M. Rogawski,et al.  Kainate receptor-mediated heterosynaptic facilitation in the amygdala , 2001, Nature Neuroscience.

[34]  Andreas Lüthi,et al.  Dendritic Spine Heterogeneity Determines Afferent-Specific Hebbian Plasticity in the Amygdala , 2005, Neuron.

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

[36]  Torfi Sigurdsson,et al.  Long‐term potentiation in freely moving rats reveals asymmetries in thalamic and cortical inputs to the lateral amygdala , 2003, The European journal of neuroscience.

[37]  Joseph E LeDoux,et al.  The Group I Metabotropic Glutamate Receptor mGluR5 Is Required for Fear Memory Formation and Long-Term Potentiation in the Lateral Amygdala , 2002, The Journal of Neuroscience.

[38]  D. Kullmann,et al.  Extrasynaptic Glutamate Spillover in the Hippocampus: Dependence on Temperature and the Role of Active Glutamate Uptake , 1997, Neuron.

[39]  F. Mascagni,et al.  Corticoamygdaloid and corticocortical projections of the rat temporal cortex: APhaseolus vulgaris leucoagglutinin study , 1993, Neuroscience.

[40]  R. Richardson,et al.  Connectivity Patterns Revealed by Mapping of Active Inputs on Dendrites of Thalamorecipient Neurons in the Auditory Cortex , 2009, The Journal of Neuroscience.

[41]  Joseph E LeDoux,et al.  Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  N. Emptage,et al.  The role of the endoplasmic reticulum Ca2+ store in the plasticity of central neurons. , 2006, Trends in pharmacological sciences.

[43]  Michael Davis,et al.  Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear- potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  G. Collingridge,et al.  Kainate receptors are involved in synaptic plasticity , 1999, Nature.

[45]  Joseph E LeDoux,et al.  Response properties of single units in areas of rat auditory thalamus that project to the amygdala , 2004, Experimental Brain Research.

[46]  Eric R Kandel,et al.  Postsynaptic Induction and PKA-Dependent Expression of LTP in the Lateral Amygdala , 1998, Neuron.

[47]  Joseph E LeDoux,et al.  NMDA Receptors and L-Type Voltage-Gated Calcium Channels Contribute to Long-Term Potentiation and Different Components of Fear Memory Formation in the Lateral Amygdala , 2002, The Journal of Neuroscience.

[48]  G. Quirk,et al.  Neuronal signalling of fear memory , 2004, Nature Reviews Neuroscience.

[49]  S. Ozawa,et al.  Blocking effect of 1-naphthyl acetyl spermine on Ca2+-permeable AMPA receptors in cultured rat hippocampal neurons , 1997, Neuroscience Research.

[50]  E. Kandel,et al.  Synaptically released zinc gates long-term potentiation in fear conditioning pathways , 2006, Proceedings of the National Academy of Sciences.

[51]  Joseph E LeDoux,et al.  Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: Parallel recordings in the freely behaving rat , 1995, Neuron.