Single-unit recording and micropressure ejection techniques were used to test the effects of norepinephrine (NE) on the responses of neurons in the superficial layers (the stratum griseum superficiale and stratum opticum) of the hamster's superior colliculus (SC). Application of NE suppressed visually evoked responses by ≥30% in 75% of 40 neurons tested and produced ≥30% augmentation of responses in only 5%. The decrement in response strength was mimicked by application of the α2 adrenoceptor agonist, p-aminoclonidine, the nonspecific β agonist, isoproterenol, and the β1 agonist, dobutamine. These agents had similar effects on responses evoked by electrical stimulation of the optic chiasm and visual cortex. The α1 agonist, methoxamine, augmented the light-evoked responses of 53% of 49 SC cells by ≥30%, but had little effect on responses evoked by electrical stimulation of optic chiasm or visual cortex. The effects of adrenergic agonists upon the glutamate-evoked responses of SC cells that were synaptically “isolated” by concurrent application of Mg2+ were similar to those obtained during visual stimulation. Analysis of effects of NE on visually evoked and background activity indicated that application of this amine did not significantly enhance signal-to-noise ratios for most superficial layer SC neurons, and signal-to-noise ratios were in some cases reduced. These results indicate that NE acts primarily through α2 and β1 receptors to suppress the visual responses of SC neurons. Activation of either of these receptors reduces the responses of SC neurons to either of their two major visual inputs as well as to direct stimulation by glutamate, and it would thus appear that these effects are primarily postsynaptic.

Intracellular recording techniques were used to evaluate the effects of norepinephrine (NE) on the membrane properties of superficial layer (stratum griseum superficiale and stratum opticum) superior colliculus (SC) cells. Of the 207 cells tested, 44.4% (N = 92) were hyperpolarized by ≥3 mV and 8.7% (N = 18) were depolarized by ≥3 mV by application of NE. Hyperpolarization induced by NE was dose dependent (EC50 = 8.1 μM) and was associated with decreased input resistance and outward current which had a reversal potential of −94.0 mV. Depolarization was associated with a very slight rise in input resistance and had a reversal potential of −93.1 mV for the single cell tested. Pharmacologic experiments demonstrated that isoproterenol, dobutamine, and p-aminoclonidine all hyperpolarized SC cells. These results are consistent with the conclusion that NE-induced hyperpolarization of SC cells is mediated by both α2 and β1 adrenoceptors. The α1 adrenoceptor agonists, methoxamine and phenylephrine, depolarized 35% (6 of 17) of the SC cells tested by ≥3 mV. Most of the SC cells tested exhibited responses indicative of expression of more than one adrenoceptor. Application of p-aminoclonidine or dobutamine inhibited transsynaptic responses in SC cells evoked by electrical stimulation of optic tract axons. Inhibition of evoked responses by these agents was usually, but not invariably, associated with a hyperpolarization of the cell membrane and a reduction in depolarizing potentials evoked by application of glutamate. The present in vitro results are consistent with those of the companion in vivo study which suggested that NE-induced response suppression in superficial layer SC neurons was primarily postsynaptic and chiefly mediated by both α2 and β1 adrenoceptors.