4.5 Article

Bidirectional pattern-specific plasticity of the slow afterhyperpolarization in rats: role for high-voltage activated Ca2+ channels and Ih

Journal

EUROPEAN JOURNAL OF NEUROSCIENCE
Volume 34, Issue 11, Pages 1756-1765

Publisher

WILEY
DOI: 10.1111/j.1460-9568.2011.07899.x

Keywords

Ca2+channels; gamma-related firing; h-channels; intrinsic excitability; intrinsic plasticity; theta-burst

Categories

Funding

  1. National Institutes of Mental Health [F31 MH-067445]
  2. Department of Physiology at the Medical College of Wisconsin, Milwaukee, WI

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A burst of action potentials in hippocampal neurons is followed by a slow afterhyperpolarization (sAHP) that serves to limit subsequent firing. A reduction in the sAHP accompanies acquisition of several types of learning, whereas increases in the sAHP are correlated with cognitive impairment. The present study demonstrates in vitro that activity-dependent bidirectional plasticity of the sAHP does not require synaptic activation, and depends on the pattern of action potential firing. Whole-cell current-clamp recordings from CA1 pyramidal neurons in hippocampal slices from young rats (postnatal days1424) were performed in blockers of synaptic transmission. The sAHP was evoked by action potential firing at gamma-related (50 Hz, gamma-AHP) or theta frequencies (5 Hz, theta-AHP), two firing frequencies implicated in attention and memory. Interestingly, when the gamma-AHP and theta-AHP were evoked in the same cell, a gradual potentiation of the gamma-AHP (186 +/- 31%) was observed that was blocked using Ca2+ channel blockers nimodipine (10 mu m) or ?-conotoxin MVIIC (1 mu m). In experiments that exclusively evoked the sAHP with 50 Hz firing, the gamma-AHP was similarly potentiated (198 +/- 44%). However, theta-burst firing pattern alone resulted in a decrease (65 +/- 19%) of the sAHP. In these experiments, application of the h-channel blocker ZD7288 (25 mu m) selectively prevented enhancement of the gamma-AHP. These data demonstrate that induction requirements for bidirectional AHP plasticity depend on the pattern of action potential firing, and result from distinct mechanisms. The identification of novel mechanisms underlying AHP plasticity in vitro provides additional insight into the dynamic processes that may regulate neuronal excitability during learning in vivo.

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