Daily rhythmicity of large-conductance Ca2+-activated K+ currents in suprachiasmatic nucleus neurons

Jan 18, 2006Brain research

Daily patterns of calcium-activated potassium currents in brain cells controlling the body clock

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Abstract

BK channel function is elevated at night, influencing the activity of SCN neurons.

Neurons in the suprachiasmatic nucleus exhibit circadian rhythms in action potential frequency and clock gene transcription.
BK-mediated currents are a larger proportion of outward currents in SCN neurons during the night compared to the day.
The amplitude and density of BK currents are greater at night, unaffected by changes in inactivation.
The BK channel transcript KCNMA1 is present in Per1-expressing neurons and shows rhythmic expression peaking at night.
Acute inhibition of BK currents reduces the circadian rhythm of spike frequency in SCN neurons.

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Neurons within the suprachiasmatic nucleus (SCN) comprise the master circadian pacemaker in mammals. These neurons exhibit circadian rhythms in spontaneous action potential frequency and in the transcription of core circadian clock genes, including Period1 (Per1). Targeted electrophysiological recordings from SCN neurons marked with a green fluorescent protein (GFP) reporter of Per1 gene transcription have previously indicated that K(+) currents are critically involved in the expression of neurophysiological rhythmicity. The present study examined the role of large conductance, Ca(2+)-activated K(+) channels (BK) in the daily rhythmicity of mouse SCN neurons. BK-mediated currents were examined in Per1::GFP neurons under voltage clamp using iberiotoxin, a specific BK channel blocker. BK current was a greater proportion of whole-cell outward currents during the night than during the day. Analysis of iberiotoxin difference currents also demonstrated that BK current amplitude and density were greater during the night and that the day/night difference in steady state amplitude was not due to altered inactivation. Single cell RT-PCR demonstrated the presence of the BK channel transcript, KCNMA1, in Per1-expressing neurons. In situ hybridization analysis further showed that KCNMA1 mRNA was rhythmically expressed in the SCN under light:dark (LD) conditions, peaking during the middle of the night phase. Acute inhibition of BK currents blunted the circadian rhythm SCN neuron spike frequency. These results establish that BK channel function is elevated at night, thus altering SCN neuron activity.

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Daily rhythmicity of large-conductance Ca2+-activated K+ currents in suprachiasmatic nucleus neurons

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