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The Journal of Neuroscience, May 20, 2009, 29(20):6427-6435; doi:10.1523/JNEUROSCI.0545-09.2009

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Behavioral/Systems/Cognitive
Membrane Resonance in Bursting Pacemaker Neurons of an Oscillatory Network Is Correlated with Network Frequency

Vahid Tohidi¹ and Farzan Nadim^1,2

¹Federated Department of Biological Sciences, Rutgers University, Newark, New Jersey 07102, and ²Department of Mathematical Sciences, New Jersey Institute of Technology, Newark, New Jersey 07102

Correspondence should be addressed to Farzan Nadim, Department of Mathematical Sciences, New Jersey Institute of Technology, 323 Martin Luther King Boulevard, Newark, NJ 07102. Email: farzan{at}njit.edu

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 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.

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Received Jan. 2, 2009; revised March 15, 2009; accepted April 2, 2009.

Correspondence should be addressed to Farzan Nadim, Department of Mathematical Sciences, New Jersey Institute of Technology, 323 Martin Luther King Boulevard, Newark, NJ 07102. Email: farzan{at}njit.edu

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