Development of acetylcholinesterase-positive thalamic and basal forebrain afferents to embryonic rat neocortex.
By combining anterograde and retrograde axonal tracing with AChE histochemistry, we demonstrate the sources of AChE-positive afferents to embryonic neocortex, the pathways they use, their time of arrival into cortex, and their initial invasion of the cortical plate. Acetylcholinesterase (AChE) is expressed by two populations of cortical afferents: AChE is permanently present in basal forebrain fibers and has been reported to be transiently localized in axons of the principal sensory thalamic nuclei over the first few postnatal weeks beginning at the middle of the first week. We first detect AChE-positive afferents histochemically in neocortex on embryonic day seventeen (E17) and determine that they arise from the principal sensory thalamic nuclei. AChE histochemistry labels the entire length of developing thalamocortical axons, including their growth cones and branches. These AChE-positive afferents enter the neocortex by the internal capsule and take an intracortical pathway centered on the subplate layer. As soon as these axons are detected, some have already begun to extend AChE-positive collateral branches superficially toward the cortical plate. By E19, a few collaterals have entered the deep part of the cortical plate and by E21 have densely invaded all but its most superficial undifferentiated part. AChE-positive afferents from basal forebrain structures reach the neocortex by three routes: the external capsule, the internal capsule, and the cingulate bundle. Among basal forebrain components, only the substantia innominata and nucleus basalis of Meynert reach the cortex by the internal capsule. Afferents from these two sources reach neocortex on E18, but are a very minor component of the total population of AChE-positive afferents at this age. Afferents from other basal forebrain components do not reach neocortex until several days later. The spatial and temporal patterns of AChE expression in developing thalamocortical axons indicate that it is useful for delineating their innervation of the primary sensory areas of embryonic neocortex, and suggest that AChE may function in axon extension and cortical differentiation.
De Carlos
J A
JA
Molecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, Ca 92037, USA.
Schlaggar
B L
BL
O'Leary
D D
DD
D000110:Acetylcholinesterase / Q000378:metabolism*; D000578:Amidines; D000818:Animals; D001369:Axons / Q000502:physiology; D002232:Carbocyanines; D005260:Female; D005456:Fluorescent Dyes; D006651:Histocytochemistry; D009412:Nerve Fibers / Q000201:enzymology; D009475:Neurons, Afferent / Q000201:enzymology*; D011247:Pregnancy; D016548:Prosencephalon / Q000166:cytology / Q000196:embryology* / Q000201:enzymology; D051381:Rats; D017207:Rats, Sprague-Dawley; D013788:Thalamus / Q000166:cytology / Q000196:embryology* / Q000201:enzymology
D000578:Amidines; D002232:Carbocyanines; D005456:Fluorescent Dyes; C031455:diamidino compound 253-50; C024286:3,3'-dioctadecylindocarbocyanine; D000110:Acetylcholinesterase