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The Journal of Neuroscience, May 15, 1999, 19(10):4034-4045

5-HT_1B Receptor-Mediated Presynaptic Inhibition of Retinal Input to the Suprachiasmatic Nucleus

Gary E. Pickard¹, Bret N. Smith¹, Michael Belenky², Michael A. Rea³, F. Edward Dudek¹, and Patricia J. Sollars¹

¹ Department of Anatomy and Neurobiology, Colorado State University, Fort Collins, Colorado 80523-1670, ² Department of Cell and Animal Biology, Hebrew University of Jerusalem, Jerusalem 91904, Israel, and ³ Brain Research Institute, Brooks Air Force Base, Texas 78235

The suprachiasmatic nucleus (SCN) receives glutamatergic afferents from the retina and serotonergic afferents from the midbrain, and serotonin (5-HT) can modify the response of the SCN circadian oscillator to light. 5-HT_1B receptor-mediated presynaptic inhibition has been proposed as one mechanism by which 5-HT modifies retinal input to the SCN (Pickard et al., 1996). This hypothesis was tested by examining the subcellular localization of 5-HT_1B receptors in the mouse SCN using electron microscopic immunocytochemical analysis with 5-HT_1B receptor antibodies and whole-cell patch-clamp recordings from SCN neurons in hamster hypothalamic slices. 5-HT_1B receptor immunostaining was observed associated with the plasma membrane of retinal terminals in the SCN. 1-[3-(Trifluoromethyl)phenyl]-piperazine HCl (TFMPP), a 5-HT_1B receptor agonist, reduced in a dose-related manner the amplitude of glutamatergic EPSCs evoked by stimulating selectively the optic nerve. Selective 5-HT_1A or 5-HT₇ receptor antagonists did not block this effect. Moreover, in cells demonstrating an evoked EPSC in response to optic nerve stimulation, TFMPP had no effect on the amplitude of inward currents generated by local application of glutamate. The effect of TFMPP on light-induced phase shifts was also examined using 5-HT_1B receptor knock-out mice. TFMPP inhibited behavioral responses to light in wild-type mice but was ineffective in inhibiting light-induced phase shifts in 5-HT_1B receptor knock-out mice. The results indicate that 5-HT can reduce retinal input to the circadian system by acting at presynaptic 5-HT_1B receptors located on retinal axons in the SCN.

Key words: circadian rhythms; serotonin; 5-HT_1B receptor knock-out mice; retinal ganglion cells; presynaptic; hypothalamic slice

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Copyright © 1999 Society for Neuroscience  0270-6474/99/19104034-12$05.00/0

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