Cortical projections to the superior colliculus in prosimian galagos (Otolemur garnetti)

Abstract

The superior colliculus (SC) is a key structure within the extrageniculate pathway of visual information to cortex and is highly involved in visuomotor functions. Previous studies in anthropoid primates have shown that superficial layers of the SC receive direct inputs from various visual cortical areas such as V1, V2, and middle temporal (MT), while deeper layers receive direct inputs from visuomotor cortical areas within the posterior parietal cortex and the frontal eye fields. Very little is known, however, about the corticotectal projections in prosimian primates. In the current study we investigated the sources of cortical inputs to the SC in prosimian galagos (Otolemur garnetti) using retrograde anatomical tracers placed into the SC. The superficial layers of the SC in galagos received the majority of their inputs from early visual areas and visual areas within the MT complex. Yet, surprisingly, MT itself had relatively few corticotectal projections. Deeper layers of the SC received direct projections from visuomotor areas including the posterior parietal cortex and premotor cortex. However, relatively few corticotectal projections originated within the frontal eye fields. While prosimian galagos resemble other primates in having early visual areas project to the superficial layers of the SC, with higher visuomotor regions projecting to deeper layers, the results suggest that MT and frontal eye field projections to the SC were sparse in early primates, remained sparse in present-day prosimian primates, and became more pronounced in anthropoid primates.

Figure 1

Cortical organization of prosimian galagos and tracer injection methods. A: The current understanding of cortical organization of prosimian galagos based on Fang et al. (2005) and Kaas and Lyon (2002). Areas include primary visual area (V1), secondary visual area (V2), the third visual area (V3), dorsomedial area (DM), dorsolateral area (DL), middle temporal area (MT), middle temporal crescent (MTc), medial superior temporal sulcus (MST), the fundus of the superior temporal sulcus (FST), inferior temporal cortex (IT), auditory cortex (A), primary somatosensory cortex (3b/S1), motor cortex (M), premotor dorsal area (PMD), premotor ventral area (PMV), orbital frontal cortex (Of), and the granular frontal cortex (Gr). LS is the lateral sulcus, IPS is the intraparietal sulcus, and FS indicates the frontal sulci. B: A dorsal view of the galago brain showing the location of the lesion in the left hemisphere in order to access the superior colliculus for injections. C: A close-up view of the aspirated cortex with a view of the superior colliculus. The right hemisphere was retracted slightly in order to view and inject the right superior colliculus.

Figure 2

Coronal sections of the superior colliculus stained for cytochrome oxidase (CO: A) or acetylcholinesterase (AChE: B). Photographs are taken from two different galagos. SZ, stratum zonale; SGS, stratum griseum superficiale; SO, stratum opticum; SGI, stratum griseum intermediale; SAI, stratum album interme-diale; SGP, stratum griseum profundum; SAP, stratum album pro-fundum. Medial is left. Scale bar = 1 mm.

Figure 3

Cortical projections to the superficial and intermediate layers of the superior colliculus (SC) in case 07–111. A: The distribution of retrogradely labeled cells within flattened cortex after a fluoro-ruby (FR) injection into the SC. Gray dots represent FR cells. Solid lines represent borders determined using CO or myelin stains while dashed lines are estimated borders based on measurements and locations relative to other landmarks. The gray shaded area is cortex that was within sulci or along the medial or ventral surfaces. B: Dorsal view of the SC with the location of the FR injection site. C: Photomicrograph of the injection site within the SC. D: Photomicrograph of the adjacent section stained for CO. Scale bars = 5 mm in A; 0.5 mm in C,D.

Figure 4

Cortical projections to the superficial and intermediate layers of the SC in case 08–40. A: Reconstruction of CTB-labeled cells in flattened cortex. B: Dorsal view of the injection site within the SC. C: Photomicrograph of a section stained for myelin indicating the location of MT, MST, MTc, and FST. D: Close-up view of the labeled cells within the MT complex region. Scale bars = 5 mm in A; 2 mm in C,D.

Figure 5

Cortical projections to the superficial and intermediate layers of the SC in case 07–105. A: The distribution of retrogradely labeled cortical cells in flattened cortex after injections into the superficial and intermediate layers of the SC. Red dots represent retrogradely labeled cells from the FR injections while black dots represent retrogradely labeled cells from the CTB injection site. B: Our reconstruction of the injection sites on a dorsal view of the SC, with red representing the FR injection site and gray representing the CTB injection site. Visuotopic information is based on Lane et al. (1973). C: A photomicrograph of a coronal section of the SC with part of the CTB injection site. The injection site is mainly limited to the superficial layers of the SC. D: A photomicrograph of the coronal section of the superior colliculus with part of the FR injection site with the injection site located within superficial and intermediate layers of the SC. E: A photomicrograph of a myelin section showing the location of MT, MTS, FST, and MTc. F: Close-up view of the location of retrogradely labeled cells with respect to E. Scale bars = 5 mm in A; 0.5 mm in C,D; 2 mm in E,F.

Figure 6

Cortical projections to superficial, intermediate, and deep layers of the SC in case 09–34. A: The distribution of CTB (black) and FR (red) retrogradely labeled cells within flattened cortex after injections into the superior colliculus that involved superficial, intermediate, and deep layers of the SC. B: Dorsal view of the SC indicating the locations of the CTB (gray), and FR (red) injection sites. C: A myelin stained section cut parallel to the brain surface showing the locations of MT, MST, FST, and MTc. D: Close-up view of the labeled cells within the MT complex region. E: Photomicrograph of the FR injection site within a coronal brain section through the SC. F: A photomicrograph of an adjacent section to E stained for CO. G: Photomicrograph of the location of the CTB injection site within a coronal view of the SC. H: Photomicrograph of the adjacent CO-stained section to G. I: Photomicrograph of CTB-labeled cells within occipital cortex. Scale bars = 5 mm in A; 2 mm in C,D; 1 mm in E–H; 50 µm in I.

Figure 7

Cortical projections to superficial, intermediate, and deep layers of the SC in case 09-03. The distribution of retrogradely labeled CTB cells within flattened cortex after a CTB injection into the deep, intermediate, and superficial layers of the SC. B: Dorsal view of the injection site within the SC. C: Photomicrograph of a coronal AChE section at the location of the injection site core within the SGI. D: Photomicrograph of a coronal section stained for CTB showing the tracer spread through the full layers of the SC. Scale bars = 5 mm in A; 1 mm in C,D.