Maturation of multisensory integration in the superior colliculus: Expression of nitric oxide synthase and neurofilament SMI-32

Abstract

Nitric oxide (NO) containing (nitrergic) interneurons are well-positioned to convey the cortical influences that are crucial for multisensory integration in superior colliculus (SC) output neurons. However, it is not known whether nitrergic interneurons are in this position early in life, and might, therefore, also play a role in the functional maturation of this circuit. In the present study, we investigated the postnatal developmental relationship between these two populations of neurons using B-nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH) histochemistry and SMI-32 immunocytochemistry to label presumptive interneurons and output neurons, respectively. SMI-32 immunostained neurons were proved to mature and retained immature anatomical features until approximately 8 postnatal weeks. In contrast, nitrergic interneurons developed more rapidly. They had achieved their adult-like anatomy by 4 postnatal weeks and were in a position to influence the dendritic elaboration of output neurons. It is this dendritic substrate through which much of the cortico-collicular influence is expressed. Double-labeling experiments showed that the dendritic and axonal processes of nitrergic interneurons already apposed the somata and dendrites of SMI-32 labeled neurons even at the earliest age examined. The results suggest that nitrergic interneurons play a role in refining the cortico-collicular projection patterns that are believed to be essential for SC output neurons to engage in multisensory integration and to support normal orientation responses to cross-modal stimuli.

Pattern of nitrergic cells and fibers organization in the central nervous system of the Australian lungfish,Neoceratodus forsteri(Sarcopterygii: Dipnoi)

“…In addition, nitrergic cells have been also described in outer tectal layers of chondrostean fishes and birds (Atoji et al, ; Brüning, ; Cozzi et al, ; Pushchina & Obukhov, ; Scicolone et al, ). In mammals, nitrergic cells are distributed in inner, intermediate and outer layers of the superior colliculus (Egberongbe et al, ; Mizukawa et al, ; Vincent & Kimura, ), and have been proposed to be interneurons that convey cortical influences onto superior colliculus output neurons (Fuentes‐Santamaria, McHaffie, & Stein, ).…”

Organization of the nitrergic neuronal system in the primitive bony fishesPolypterus senegalusandErpetoichthys calabaricus(Actinopterygii: Cladistia)

“…In birds, the nitrergic cells are present in inner periventricular and outer layers (Brüning, ; Cozzi et al, ; Atoji et al, ; Scicolone et al, ), whereas, in mammals, in addition to the nitrergic cell bodies in inner locations, these cells are also present in intermediate and superficial layers of the superior colliculus (Mizukawa et al, ; Vincent and Kimura, ; Egberongbe et al, ). The optic tectum/superior colliculus is an important brain structure involved not only in the processing of visual information but also in multisensory integration, and for mammals the nitrergic cells have been proposed to be interneurons positioned to convey cortical influences onto superior colliculus output neurons (Fuentes‐Santamaría et al, ).…”

Development of multisensory integration from the perspective of the individual neuron

“…Unfortunately, although the projection patterns have begun to be evaluated 113,114 , little is known about the morphology of the cortico-collicular synaptic configurations on multisensory neurons or how and when they develop. Cortico-collicular inputs from at least some regions of the association cortex are already present within days of birth 115 and presumably during late embryonic stages, but their synaptic inputs are likely to be unformed or non-functional.…”