Dendritic SK channels convert NMDA-R-dependent LTD to burst timing-dependent plasticity

J Neurophysiol. 2013 Dec;110(12):2689-703. doi: 10.1152/jn.00506.2013. Epub 2013 Sep 18.

Abstract

Feedback and descending projections from higher to lower brain centers play a prominent role in all vertebrate sensory systems. Feedback might be optimized for the specific sensory processing tasks in their target brain centers, but it has been difficult to connect the properties of feedback synapses to sensory tasks. Here, we use the electrosensory system of a gymnotiform fish (Apteronotus leptorhynchus) to address this problem. Cerebellar feedback to pyramidal cells in the first central electrosensory processing region, the electrosensory lateral line lobe (ELL), is critical for canceling spatially and temporally redundant electrosensory input. The ELL contains four electrosensory maps, and we have previously analyzed the synaptic and network bases of the redundancy reduction mechanism in a map (centrolateral segment; CLS) believed to guide electrolocation behavior. In the CLS, only long-term depression was induced by pairing feedback presynaptic and pyramidal cell postsynaptic bursts. In this paper, we turn to an ELL map (lateral segment; LS) known to encode electrocommunication signals. We find remarkable differences in synaptic plasticity of the morphologically identical cerebellar feedback input to the LS. In the LS, pyramidal cell SK channels permit long-term potentiation (LTP) of feedback synapses when pre- and postsynaptic bursts occur at the same time. We hypothesize that LTP in this map is required for enhancing the encoding of weak electrocommunication signals. We conclude that feedback inputs that appear morphologically identical in sensory maps dedicated to different tasks, nevertheless display different synaptic plasticity rules contributing to differential sensory processing in these maps.

Keywords: NMDA receptor; SK channel; STDP; action potential burst; cerebellum; communication signal; electrosensory system; parallel fibers; sensory processing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials
  • Animals
  • Cerebellum / cytology
  • Cerebellum / physiology
  • Dendrites / metabolism*
  • Dendrites / physiology
  • Electric Organ / innervation
  • Electric Organ / physiology
  • Excitatory Postsynaptic Potentials
  • Feedback, Physiological
  • Gymnotiformes
  • Long-Term Potentiation
  • Long-Term Synaptic Depression*
  • Pyramidal Cells / metabolism
  • Pyramidal Cells / physiology*
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Small-Conductance Calcium-Activated Potassium Channels / metabolism*

Substances

  • Receptors, N-Methyl-D-Aspartate
  • Small-Conductance Calcium-Activated Potassium Channels