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The Suprachiasmatic Nucleus Exhibits Diurnal Variations in Spontaneous Excitatory Postsynaptic Activity

Krister Kristensson

Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden

Russell H. Hill

Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden; Russell.Hill{at}neuro.ki.se

A most prominent feature of neurons in the suprachiasmatic nucleus (SCN) is the circadian rhythm in spontaneous firing frequency. To disclose synaptic mechanisms associated with the rhythmic activity, the spontaneous postsynaptic activity was studied using whole-cell, patch clamp recordings in the ventral region of the SCN in slice preparations from rats. The synaptic events were compared between two time intervals corresponding to the highest and lowest electrical activity within the SCN during subjective daytime and nighttime, respectively. The [.gamma]-aminobutyric acid (GABA)–mediated spontaneous inhibitory activity showed no diurnal variations, but the excitatory activity was markedly higher in frequency, without differences in amplitude, during the subjective day compared to the subjective night. Spontaneous and evoked inhibitory synaptic events were blocked by the GABA_A receptor antagonist bicuculline. The [.alpha]-amino-hydroxy-5-methylisoxazole-4-propionic acid (AMPA/kainate) receptor antagonist 6-cyano-7-nitroquinoxaline-2, 3-dione (CNQX) blocked most of the excitatory activity. In addition, CNQX reduced the spontaneous inhibitory activity. The N-methyl-D-aspartate antagonist D-2-amino-5-phosphonopentanoic acid reduced the inhibitory activity to a lesser degree, and there was no significant difference in amplitude or frequency of synaptic events in control and Mg²⁺-free solutions, indicating that the AMPA receptor plays an important role in regulating the inhibitory release of GABAwithin the SCN. Ipsiand contralateral stimulation of the SCN consistently evoked excitatory synaptic responses. Inhibitory synaptic responses occurred in some neurons upon increasing stimulus strength. In conclusion, this study shows that there is a substantial influence from spontaneous glutamatergic synapses on the ventral part of the SCN and that these exhibit daily variations in activity. Diurnal fluctuations in spontaneous excitatory postsynaptic activity within this network may contribute to the mechanisms for synchronization of rhythms between individual SCN neurons and may underlie the daily variations in the spontaneous firing frequency of SCN neurons.

Key Words: suprachiasmatic nucleus (SCN) • circadian rhythm • spontaneous synaptic activity • slice • patch clamp • glutamate • [.gamma]-aminobutyric acid (GABA) • [.alpha]-amino-hydroxy-5-methylisoxazole-4-propionic acid (AMPA)

Journal of Biological Rhythms, Vol. 17, No. 1, 40-51 (2002)
DOI: 10.1177/074873002129002320


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