Nigral inhibitory termination on efferent neurons of the superior colliculus: an intracellular horseradish peroxidase study in the cat.

Abstract

Intracellularly recorded responses of deeper tectal neurons to stimulation of the substantia nigra and the cerebral peduncle were obtained to demonstrate the monosynaptic inhibitory nature of the nigrotectal pathway in the cat. We also employed antidromic stimulation (contralateral predorsal bundle and superior colliculus) and intracellular labeling with HRP to demonstrate which types of tectal efferent neurons are nigrorecipient. The response to nigral stimulation in 61% of the cells studied was a monosynaptic IPSP of short duration. Recovered HRP-labeled nigrorecipient neurons include X1 (large multipolar radiating), X2 (tufted), X4 (medium-size vertical), X5 (medium-size horizontal), T1 (medium-size trapezoid radiating), T2 (small ovoid vertical), I (small sparsely ramified), and A (small horizontal) neurons. Nigrorecipient cells participate in all four of the major efferent axonal systems of the deeper tectal layers: crossed descending (X and T neurons), ipsilateral descending (I and T neurons), ascending (A, X, and T neurons), and commissural (T neurons). EPSPs accompanied by long-lasting hyperpolarizing potentials were recorded from the remaining tectal neurons in response to stimulation of the substantia nigra, cerebral peduncle, and pericruciate cortex. Collision experiments indicate that at least part of the excitatory responses of tectal neurons to nigral and penduncular stimulation are mediated by corticotectal fibers traversing the cerebral peduncle and the substantia nigra. Excitatory effects of nigral, peduncular, and cortical stimulation were disclosed in X neurons including the non-nigrorecipient large vertical neurons of the X3 subgroup. Cortical excitatory and nigral inhibitory inputs converge only on X neurons (X1, X2, X4, X5). In this case, nigrally evoked IPSPs were preceded by a brief EPSP. Collectively, these results demonstrate the inhibitory termination of the nigrotectal pathway on a wide variety of deeper tectal efferent neurons. Such findings imply the versatility of the nigral involvement in tectal mechanisms of gaze control. We suggest that the substantia nigra pars reticulata contacts tectal neurons differing as to their response properties and shapes the signal carried by all the major tectofugal bundles.