Membrane resonance in bursting pacemaker neurons of an oscillatory network is correlated with network frequency

J Neurosci. 2009 May 20;29(20):6427-35. doi: 10.1523/JNEUROSCI.0545-09.2009.

Abstract

Network oscillations typically span a limited range of frequency. In pacemaker-driven networks, including many central pattern generators (CPGs), this frequency range is determined by the properties of bursting pacemaker neurons and their synaptic connections; thus, factors that affect the burst frequency of pacemaker neurons should play a role in determining the network frequency. We examine the role of membrane resonance of pacemaker neurons on the network frequency in the crab pyloric CPG. The pyloric oscillations (frequency of approximately 1 Hz) are generated by a group of pacemaker neurons: the anterior burster (AB) and the pyloric dilator (PD). We examine the impedance profiles of the AB and PD neurons in response to sinusoidal current injections with varying frequency and find that both neuron types exhibit membrane resonance, i.e., demonstrate maximal impedance at a given preferred frequency. The membrane resonance frequencies of the AB and PD neurons fall within the range of the pyloric network oscillation frequency. Experiments with pharmacological blockers and computational modeling show that both calcium currents I(Ca) and the hyperpolarization-activated inward current I(h) are important in producing the membrane resonance in these neurons. We then demonstrate that both the membrane resonance frequency of the PD neuron and its suprathreshold bursting frequency can be shifted in the same direction by either direct current injection or by using the dynamic-clamp technique to inject artificial conductances for I(h) or I(Ca). Together, these results suggest that membrane resonance of pacemaker neurons can be strongly correlated with the CPG oscillation frequency.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology*
  • Animals
  • Biological Clocks / physiology*
  • Brachyura
  • Computer Simulation
  • Electric Stimulation / methods
  • Ganglia, Invertebrate / cytology
  • Male
  • Models, Neurological
  • Nerve Net / physiology*
  • Neural Pathways / physiology
  • Neurons / drug effects
  • Neurons / physiology*
  • Nonlinear Dynamics
  • Patch-Clamp Techniques
  • Periodicity*
  • Potassium Channel Blockers / pharmacology
  • Pylorus / physiology
  • Sodium Channel Blockers / pharmacology
  • Tetraethylammonium / pharmacology
  • Tetrodotoxin / pharmacology

Substances

  • Potassium Channel Blockers
  • Sodium Channel Blockers
  • Tetrodotoxin
  • Tetraethylammonium