Cortical somatosensory and trigeminal inputs to the cat superior colliculus: Light and electron microscopic analyses

Abstract

Two different axonal transport tracers were used in single animals to test the hypothesis that the expansive intermediate gray layer of the cat superior colliculus (stratum griseum intermediale, SGI) is composed of sensorimotor domains. The results show that two sensory pathways, the trigeminotectal and the corticotectal arising from the fourth somatosensory area, commingle in patches across the middle tier of the SGI. Furthermore, the data reveal that tectospinal cells are distributed within these patches. Taken together, these results show a commingling of functionally related afferents and a consistent spatial relationship between these afferents and tectospinal neurons. These relationships indicate that the SGI consists of domains that can be distinguished by their unique combinations of afferent and efferent connections. The ultrastructural characteristics and synaptic relationships of these somatosensory afferent pathways suggest that they have distinct roles within the sensorimotor domain of the SGI. The trigeminotectal terminals are relatively small, contain round vesicles and make asymmetrical synapses on small, presumably distal, dendrites. We submit that these trigeminal terminals bestow the basic receptive field properties upon SGI neurons. In contrast, the somatosensory corticotectal terminals are relatively large, contain round vesicles, make asymmetrical synapses, participate in triads, and are presynaptic to proximal dendrites. We suggest that these cortical terminals bestow integrative abilities on SGI neurons.

Comparison of the ultrastructure of cortical and retinal terminals in the rat superior colliculus

“…Corticotectal terminals in the deeper layers of the cat SC, labeled by tritiated amino acid injections in the dorsal bank of the anterior ectosylvian sulcus, were observed to be relatively large terminals (diameter, 2.16 Ϯ 0.30) (Harting et al, 1997). Therefore, corticotectal terminal morphology may also vary with cortical area of origin.…”

Somatosensory areas S2 and PV project to the superior colliculus of a prosimian primate,Galago garnetti

“…The somatosensory inputs could come from any of a number of sources. In rodents (e.g., Rhoades et al 1981) and carnivores (e.g., Harting et al 1997), there is evidence for a direct relay of somatosensory information to the superior colliculus from the dorsal-columntrigeminal complex. A somatosensory representation in the zona incerta provides another source of direct input (e.g., Nicolelis et al 1992).…”

“…However, there have been some important observations. In cats, a higher-order somatosensory area, termed S4 (Clemo and Stein 1983), and adjacent cortex of the anterior ectosylvian sulcus, AES, project to the superior colliculus Clemo and Stein 1984;McHaffie et al 1988;Harting et al 1992;Harting et al 1997). However, there is no clear evidence ) for projections to the superior colliculus from other somatosensory areas in cats (S1, S2, and S3), and S4 has no obvious homologue in mammals other than carnivores.…”

Adaptation in multisensory neurons: Impact on cross-modal enhancement

“…In particular, when these two cortical areas are deactivated by cooling, cross-modal enhancement is reversibly eliminated while unimodal responses, although perhaps somewhat attenuated, remain largely intact (Wallace and Stein 2000;Jiang et al 2001;Stein 2005;Jiang et al 2006;Alvarado et al 2007). Furthermore, electron microscope studies suggest that there is a close juxtaposition of the descending, cortical projections with the ascending, sensory inputs on the dendrites of deep superior colliculus neurons (Harting et al 1997). Such a juxtaposition could underlie the computation of the correlation coefficients between different sensory channels' activities.…”