Plasticity of Light-induced Concurrent Glutamatergic and GABAergic Quantal Events in the Suprachiasmatic Nucleus.

Neurons in the suprachiasmatic nucleus (SCN) exhibit circadian variation in their neuronal activities. Here, we show that their input synapses undergo daily regulation. We discovered daily variation in the frequencies, but not the peak amplitudes, of miniature postsynaptic currents (mPSCs) for both glutamatergic and GABAergic synapses. In addition, the changes in the frequencies of mPSCs from glutamatergic and GABAergic synapses were antiphasic: An increase in the glutamatergic mPSC frequency and a decrease in the GABAergic mPSC frequency co-occurred during the dark phase of the light-dark cycle. Through optogenetic stimulation of presynaptic glutamatergic axonal terminals, we demonstrated that the elicited quantal size glutamatergic PSC could evoke action potentials in postsynaptic SCN neurons with higher probability during the light phase than during the dark phase. To investigate whether the intrinsic clock or the light-dark cycle mediates the daily rhythm of input synapses, we examined the mPSCs under light masking and skeleton photoperiod schemes. A prolonged light pulse (3 h) at the beginning of the subjective night suppressed the changes in mPSCs frequencies for both glutamatergic and GABAergic synapses; under the skeleton photoperiod, no significant differences were observed in mPSCs frequencies between the subjective day and night. Furthermore, we discovered that the plasticity of these concurrent quantal events occurred primarily in vasoactive intestinal peptide (VIP) neurons. This work provides evidence for light-dependent synaptic plasticity at glutamatergic and GABAergic input synapses of ventral SCN neurons. This concurrent synaptic plasticity could serve as one mechanism for regulating the responsiveness of SCN neurons to the wide range of light input over the day and night.