Fast multisite optical recording of mono- and polysynaptic activity in the hamster suprachiasmatic nucleus evoked by retinohypothalamic tract stimulation.

Responses of the hamster suprachiasmatic nucleus (SCN) to retinohypothalamic tract (RHT) stimulation were studied in horizontal hypothalamic slices using fast multisite optical recording techniques. A 124-element photodiode detector array provided high-speed monitoring (0.5 ms/frame) of evoked neural activity in the SCN, while a larger 464-element photodiode array yielded improved spatial imaging with some loss in temporal resolution (1.6 ms/frame). Brief electrical stimulation of the optic nerves evoked a propagated compound action potential that was recorded optically as a single transient depolarization in many slice regions, including the SCN. Only within the SCN, however, was this optic tract signal followed by additional voltage-dependent optical responses which exhibited a fast and a slow depolarizing component. The initial upstroke of the fast component was Ca(2+)-insensitive and is presumed to reflect activity in presynaptic RHT afferents. The remainder of the fast depolarization and the slow depolarization were Ca(2+)-sensitive. These responses were labeled the early population excitatory postsynaptic potential (Early P.E.P.S.P.) and the Late P.E.P.S.P. respectively. The Late P.E.P.S.P. was not enhanced by K+ channel blockade, suggesting that glial depolarization is not the primary source of this component. Drugs known to suppress RHT-evoked SCN field potentials also suppressed the Early and Late P.E.P.S.P.'s recorded optically in the SCN. Unexpectedly, the Early P.E.P.S.P. was also reduced by the GABAA antagonist, bicuculline. Surface plots of normalized peak amplitudes showed that both SCN components had similar spatial distributions within the SCN, although the Early P.E.P.S.P. tended to be slightly more prominent within the medial SCN in some preparations. It is suggested that the Early P.E.P.S.P. represents firing of monosynaptically activated SCN neurons, while the Late P.E.P.S.P. reflects polysynaptic activity within the intrinsic SCN neuronal network that may be involved in the light entrainment of the circadian oscillator.