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The Journal of Neuroscience, October 24, 2007, 27(43):11748-11757; doi:10.1523/JNEUROSCI.1840-07.2007

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Behavioral/Systems/Cognitive
Calcium Response to Retinohypothalamic Tract Synaptic Transmission in Suprachiasmatic Nucleus Neurons

Robert P. Irwin and Charles N. Allen

Center for Research on Occupational and Environmental Toxicology, Oregon Health & Science University, Portland, Oregon 97239

Correspondence should be addressed to Dr. Robert P. Irwin, Center for Research on Occupational and Environmental Toxicology, Oregon Health & Science University, L-606, 3181 Southwest Sam Jackson Park Road, Portland, OR 97239. Email: irwinr{at}ohsu.edu

Glutamate released from retinohypothalamic tract (RHT) synapses with suprachiasmatic nucleus (SCN) neurons induces phase changes in the circadian clock presumably by using Ca²⁺ as a second messenger. We used electrophysiological and Ca²⁺ imaging techniques to simultaneously record changes in the membrane potential and intracellular calcium concentration ([Ca²⁺]_i) in SCN neurons after stimulation of the RHT at physiologically relevant frequencies. Stimulation of the RHT sufficient to generate an EPSP did not produce detectable changes in [Ca²⁺]_i, whereas EPSP-induced action potentials evoked an increase in [Ca²⁺]_i, suggesting that the change in postsynaptic somatic [Ca²⁺]_i produced by synaptically activated glutamate receptors was the result of membrane depolarization activating voltage-dependent Ca²⁺ channels. The magnitude of the Ca²⁺ response was dependent on the RHT stimulation frequency and duration, and on the SCN neuron action potential frequency. Membrane depolarization-induced changes in [Ca²⁺]_i were larger and decayed more quickly in the dendrites than in the soma and were attenuated by nimodipine, suggesting a compartmentalization of Ca²⁺ signaling and a contribution of L-type Ca²⁺ channels.

RHT stimulation at frequencies that mimicked the output of light-sensitive retinal ganglion cells (RGCs) evoked [Ca²⁺]_i transients in SCN neurons via membrane depolarization and activation of voltage-dependent Ca²⁺ channels. These data suggest that for Ca²⁺ to induce phase advances or delays, light-induced signaling from RGCs must augment the underlying oscillatory somatic [Ca²⁺]_i by evoking postsynaptic action potentials in SCN neurons during a period of slow spontaneous firing such as occurs during nighttime.

Key words: circadian rhythm; suprachiasmatic nucleus; action potential; retinal ganglion cells; synaptic transmission; calcium

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Received April 23, 2007; revised Aug. 16, 2007; accepted Sept. 12, 2007.

Correspondence should be addressed to Dr. Robert P. Irwin, Center for Research on Occupational and Environmental Toxicology, Oregon Health & Science University, L-606, 3181 Southwest Sam Jackson Park Road, Portland, OR 97239. Email: irwinr{at}ohsu.edu

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