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Learning-dependent plasticity of hippocampal CA1 pyramidal neuron postburst afterhyperpolarizations and increased excitability after inhibitory avoidance learning depend upon basolateral amygdala inputs

Authors

  • George E. Farmer,

    1. Cognition and Neuroscience Program, School of Behavioral and Brain Sciences, the University of Texas at Dallas, Richardson, Texas
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  • Lucien T. Thompson

    Corresponding author
    1. Cognition and Neuroscience Program, School of Behavioral and Brain Sciences, the University of Texas at Dallas, Richardson, Texas
    • L.T. Thompson, GR4.1, School of Behavioral and Brain Sciences, University of Texas at Dallas, 800 W. Campbell Rd., Richardson, TX 75080, USA
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Abstract

Hippocampal pyramidal neurons in vitro exhibit transient learning-dependent reductions in the amplitude and duration of calcium-dependent postburst afterhyperpolarizations (AHPs), accompanied by other increases in excitability (i.e., increased firing rate, or reduced spike-frequency accommodation) after trace eyeblink conditioning or spatial learning, with a time-course appropriate to support consolidation of the learned tasks. Both these tasks require multiple days of training for acquisition. The hippocampus also plays a role in acquisition of single trial inhibitory avoidance learning. The current study assessed AHP plasticity in this single-trial learning task using in vitro tissue slices prepared at varying intervals posttrial using intracellular current-clamp recordings. Reduced AHPs and reduced accommodation were seen in ventral CA1 pyramidal neurons within 1 h posttraining, plasticity which persisted 24 h but was extinguished >72 h posttrial. There was also a reduction in ventral CA1 AHPs and accommodation 1 h following simple exposure to the IA apparatus (a novel context) but this change was extinguished by 24 h postexposure. Reductions in AHPs and accommodation were also seen in dorsal CA1 pyramidal neurons, but were delayed until 24 h posttrial and extinguished at >72 h posttrial. Finally, transient inactivation of the basolateral complex of the amygdala (with the local anesthetics lidocaine or bupivacaine) either immediately before or immediately posttrial blocked both learning and learning-dependent changes in excitability in the hippocampus assessed 24 h posttrial. CA3 pyramidal neurons showed no reductions in AHP peak amplitude or accommodation following IA training or context exposure. © 2012 Wiley Periodicals, Inc.

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