Connection from the dorsal column nuclei to the superior colliculus in the rat: Topographical organization and somatotopic specific plasticity in response to neonatal enucleation

Abstract

Somatosensory stimuli from the body to deep and intermediate strata of the superior colliculus (SC) are relayed from the dorsal column nuclei (DCN), gracile (GrN) and cuneate (CuN). Electrophysiological studies have shown that the somatosensory representation in SC is arranged into a map-like pattern. However, there is a lack of studies confirming a morphological correlate of such an organization. On the other hand, after neonatal enucleation in rodents, somatosensory inputs ascend from their normal termination territory in intermediate and deep collicular strata to invade the more dorsally located visual strata. However, the origin of these reactive afferents has not been specified. By using anterograde (biotinylated dextran amine 10,000; BDA) and retrograde (Fluoro-Gold; FG) tracers, we studied separately the connection from GrN and CuN to the intact and neonatally deafferented SC. GrN-collicular afferents were found to terminate mainly within the periphery of the caudomedial SC quadrant, whereas CuN-collicular fibers innervated primarily the lateral part of the rostrolateral and caudolateral collicular quadrants, in a way consistent with previously described functional data. Retrograde tracing experiments using FG injected in SC confirmed this topographical arrangement. Injections of BDA in GrN or CuN of neonatally enucleated rats showed that reactive fibers reaching superficial strata are only those CuN-collicular fibers innervating the caudolateral SC quadrant, where the forelimb is represented. The present results provide an anatomical substrate for the known somatotopic organization of tactile representation in SC and further reinforce the previous proposal that the plastic reorganization of DCN-collicular afferents following neonatal enucleation constitutes a functional compensatory response.

Functional organization and connectivity of the dorsal column nuclei complex reveals a sensorimotor integration and distribution hub

“…Surrounding the cerebral aqueduct in the tegmentum, the periaqueductal gray (PAG) receives afferents from the spinothalamic tract that transmit pain and temperature information. Interestingly, the DCN have also been shown to send contralateral projections via the ML LAC to the PAG (Figure 7; Barbaresi & Mensà, 2016; Björkeland & Boivie, 1984; García Del Caño, Uria, Gerrikagoitia, & Martínez‐Millán, 2004; Hazlett et al, 1972; Schroeder & Jane, 1971; Villanueva et al, 1998; Wiberg et al, 1987), which terminate somatotopically such that the Gr project to the caudal lateral PAG and the Cu to rostral lateral PAG (Barbaresi & Mensà, 2016).…”

Organization and origin of the connection from the inferior to the superior colliculi in the rat

“…Anatomical studies have clearly demonstrated that visual and somatosensory maps in the SC are constructed on the basis of a topographic arrangement of afferents to this structure (Nauta and van Straaten,1947; Lund et al,1980; Ndiaye et al,2002; García del Caño et al,2004). However, despite the fact that the acoustic environment is represented in a map‐like fashion, in contrast to the visual and somatosensory systems it does not appear to be based on a topographical arrangement of auditory afferent fibers (see Stein and Meredith,1993b, for review).…”

Functional Organisation and Connectivity of the Dorsal Column Nuclei Complex Reveals a Sensorimotor Integration and Distribution Hub

“…Surrounding the cerebral aqueduct in the tegmentum, the periaqueductal grey (PAG) receives afferents from the spinothalamic tract that transmit pain and temperature information. Interestingly, the DCN have also been shown to send contralateral projections via the ML LAC to the PAG (Figure 7) (Barbaresi & Mensà, 2016;Björkeland & Boivie, 1984;García Del Caño, Uria, Gerrikagoitia, & Martínez-Millán, 2004;Hazlett et al, 1972;Villanueva et al, 1998;Wiberg et al, 1987), which terminate somatotopically such that the Gr project to the caudal lateral PAG and the Cu to rostral lateral PAG (Barbaresi & Mensà, 2016).…”