Pathway from the zona incerta to the superior colliculus in the rat

Abstract

In order to test the proposal that the zona incerta contributes to the generation of orienting movements, we examined the synaptic relationships between the incertotectal pathway and the cells of origin of the predorsal bundle. The predorsal bundle cells give rise to the major premotor pathway from the superior colliculus to the brainstem gaze centers. First, cytochrome oxidase histochemistry, gamma-aminobutyric acid (GABA), and glutamic acid decarboxylase (GAD) immunocytochemistry, and the axonal transport of markers were used to define the borders of a ventral subdivision of the zona incerta. This subdivision projects topographically to the same sublamina of the intermediate grey layer of the superior colliculus that contains the vast majority of the predorsal bundle cells. Experiments in which incertotectal cells were labeled by both retrograde transport and immunocytochemistry showed that this pathway is GABAergic. Retrograde and anterograde experiments also showed that this pathway is reciprocated by a pathway from the intermediate grey layer of the superior colliculus to the same ventral subdivision of the zona incerta. Finally, experiments combining axonal transport and electron microscopic methods showed that the incertotectal pathway is the source of a monosynaptic GABAergic input to the cells of origin of the predorsal bundle. The ventral subdivision of the zona incerta is contrasted with a second source of GABAergic input to the predorsal bundle cells, the substantia nigra pars reticulata.

Nigral Inhibition of GABAergic Neurons in Mouse Superior Colliculus

“…Thus, it is most likely that the evoked IPSCs were the result of SNr stimulation and not of stimulating other structures or passing fibers. However, we cannot exclude the possibility that the IPSCs were partially derived from inputs of the zona incerta, one of the extrinsic GABAergic sources to the SC (Ficalora and Mize, 1989;Appell and Behan, 1990;Kim et al, 1992;May et al, 1997;Kolmac et al, 1998), because the part of zona incerta that projects to SGI is located adjacent to the rostral SNr (May et al, 1997). Therefore, the contribution, if any, of incertotectal inputs to the evoked IPSCs should be much smaller than that of the nigrotectal inputs.…”

“…The stimulating electrodes were placed just ventral to the SC, and repetitive stimulation (20 -50 pulses at 50 Hz) was delivered to elicit the large amount of GABA release that should be necessary for activating GABA B receptors (Isaacson et al, 1993;Mitchell and Silver, 2000;Kaneda and Kita, 2005;Kaneda et al, 2008). Although this stimulation would activate both nigral and other passing GABAergic fibers, including those from the zona incerta and reticular formation (Ficalora and Mize, 1989;Appell and Behan, 1990;Kim et al, 1992;May et al, 1997;Kolmac et al, 1998), the stimulation-evoked IPSCs were not affected by bath application of the selective GABA B receptor antagonist CGP52432 (3 M) in six of six neurons tested (Fig. 3H ).…”

Projections of somatosensory cortex and frontal eye fields onto incertotectal neurons in the cat

“…3, 4, and 11). The incertotectal pathway terminates in the intermediate gray layer of the SC [cat: May et al (1997); rat: Kim et al (1992)]. These layers contain multimodal cells, many of which display somatosensory responses [cat: Clemo and Stein (1991), Meredith et al (1991Meredith et al ( , 2000, and Stein et al (1999)].…”

“…The predominant transmitter used by the cells in both these sublaminae is GABA. For example, both the incertotectal projection from vZI [rat: Kim et al (1992) and Nicolelis et al (1992); cat: Ficalora and Mize (1989)] and the incertocortical projection from dZI [rat: Lin et al (1990) and Nicolelis et al (1992)] are GABAergic. This makes the incertotectal pathway a long-range inhibitory influence over the superior colliculus (SC), which parallels the GABAergic nigrotectal projection from pars reticulata [rat: Redgrave et al (1992); cat: Graybiel (1978), Harting et al (1988), and Ficarola and Mize (1989); squirrel: May and Hall (1984)].…”

“…This SC layer contains multisensory output cells, which project by way of the predorsal bundle to contralateral brainstem regions controlling saccadic eye movements [cat: Cowie and Holstege (1992); macaque: Harting (1977) and May and Porter (1992); rat: Dean et al (1988) and Bickford and Hall (1989); squirrel: May and Hall (1984)]. Furthermore, incertotectal terminals are found in close association with cells projecting in the predorsal bundle of rats, suggesting direct synaptic contact (Kim et al, 1992). It is precisely this subpopulation of SC output neurons that exhibit saccade-related activity [cat: Grantyn and Grantyn (1982), Moschovakis and Karabelas (1985), and Munoz and Guitton (1991); monkey: Wurtz and Goldberg (1972), Sparks and Mays (1981), and Moschovakis et al (1988)].…”