The Visuo-Motor Pathway in the Local Circuit of the Rat Superior Colliculus

Abstract

Intrinsic circuit of the superior colliculus (SC), in particular the pathway from the optic tract (OT) to neurons in the intermediate layer (SGI), was investigated by whole-cell patch-clamp recording in slice preparations obtained from 17- to 24-d-old rats. Stimulation of the OT induced monosynaptic EPSPs in neurons in the superficial gray layer (SGS) and the optic layer (SO), and disynaptic or polysynaptic EPSPs in a majority of SGI neurons. Stimulation of the SGS induced monosynaptic or oligosynaptic EPSPs in the SGI neurons. Both the monosynaptic EPSPs induced in the SGS/SO neurons by stimulation of the OT and those induced in the SGI neurons by stimulation of the SGS were mediated by AMPA- and NMDA-type glutamate receptors. Thus, we have clarified the existence of the glutamatergic excitatory pathway from the OT to the SGI neurons via SGS and SO neurons. The EPSPs in the SGI neurons induced by stimulation of the OT or SGS were remarkably enhanced by bicuculline, suggesting that the signal transmission in this pathway is under strong suppression by the GABAergic system.

GABAergic mechanisms for shaping transient visual responses in the mouse superior colliculus

“…With the use of juxtacellular labeling, we revealed that the ON + Pause + OFF responses were observed in a variety of morphological types of sSC neurons. These include WFV and NFV cells, which are reported to be excitatory neurons (Isa et al, 1998;Saito and Isa, 2005;Kaneda et al, 2008), and stellate, piriform, multipolar, and horizontal cells that are considered to be inhibitory GABAergic neurons (Mize, 1992;Endo et al, 2003;Kaneda et al, 2008). Three marginal cells, which are projection neurons (Mooney et al, 1988) and have not been characterized as GABAergic (Mize, 1992), also exhibited the ON + Pause + OFF responses.…”

“…Three marginal cells, which are projection neurons (Mooney et al, 1988) and have not been characterized as GABAergic (Mize, 1992), also exhibited the ON + Pause + OFF responses. These findings are of particular importance because both excitatory and inhibitory neurons exhibited the same response pattern, although their functions must be different from each other: as 20 excitatory sSC neurons are projection neurons (Mooney et al, 1988;Isa et al, 1998;Özen et al, 2000;Kaneda et al, 2008), they send visual information to nuclei outside the sSC. On the other hand, given that the majority of GABAergic neurons are interneurons with some exceptions (Mooney et al, 1988), their primary role is most likely to inhibit excitatory and inhibitory neurons within the sSC.…”

“…This is probably due to the high percentage of GABAergic neurons in the sSC (Okada, 1974). Thus, it is most likely that both excitatory and inhibitory neurons were included in the experiments of (Lee et al, 1997;Isa et al, 1998;Kaneda et al, 2008).…”

Nigral Inhibition of GABAergic Neurons in Mouse Superior Colliculus

“…After recording, the slices were fixed with 4% paraformaldehyde in 0.1 M phosphate buffer (PB) pH 7.4, for more than 1 d at 4°C. After fixation, biocytin-filled neurons were visualized by the avidin-biotin-peroxidase complex (ABC) method (Vectastain; Vector Laboratories), as described previously (Isa et al, 1998). The soma, dendrites, and axons of biocytin-labeled neurons were reconstructed by use of a drawing tube attached to a light microscope (BX-51; Olympus).…”

“…Burst firing in SGI neurons is probably evoked by release from nigral inhibition and concurrent cortical excitation (Isa et al, 1998;Saito and Isa, 2003;Hikosaka et al, 2006). Conversely, the burst firing might be terminated by cooperation between "reinhibition" from the SNr and the end of excitatory inputs from the cortex, as well as intrinsic excitatory interactions within the SGI (Saito and Isa, 2003).…”