Learning-dependent Plasticity of Hippocampal CA1 Pyramidal Neuron Postburst Afterhyperpolarizations and Increased Excitability After Inhibitory Avoidance Learning Depend Upon Basolateral Amygdala Inputs

Hippocampus. 2012 Aug;22(8):1703-19. doi: 10.1002/hipo.22005. Epub 2012 Feb 27.

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.

MeSH terms

  • Action Potentials / physiology*
  • Amygdala / physiology*
  • Analysis of Variance
  • Animals
  • Avoidance Learning / physiology*
  • Blinking / physiology
  • CA1 Region, Hippocampal / metabolism*
  • CA3 Region, Hippocampal / metabolism
  • Conditioning, Classical / physiology
  • Male
  • Neuronal Plasticity*
  • Pyramidal Cells / metabolism*
  • Rats
  • Rats, Long-Evans
  • Time Factors