Development of starburst cholinergic amacrine cells in the retina of Tupaia belangeri

Abstract

"Starburst" cholinergic amacrines specify the response of direction-selective ganglion cells to image motion. Here, development of cholinergic amacrines was studied in the tree shrew Tupaia belangeri (Scandentia) by immunohistochemistry with antibodies against choline acetyltransferase (ChAT) and neurofilament proteins. Starburst amacrines expressed ChAT much earlier than previously thought. From embryonic day 34 (E34) onward, orthotopic and displaced subpopulations segregated from a single cluster of immunoreactive precursor cells. Orthotopic starburst amacrines rapidly took up positions in the inner nuclear layer. Displaced starburst amacrines were first arranged in a monocellular row in the inner plexiform layer, and, with a delay of 1 week, they descended to the ganglion cell layer. Conversely, dendritic stratification of displaced amacrines slightly preceded that of orthotopic ones. Starburst amacrines expressed the medium-molecular-weight neurofilament protein (NF-M) from E34 to postnatal day 11 (P11) and coexpressed alpha-internexin from E36.5 to P11. Consequently, neurofilaments composed of alpha-internexin and NF-M may stabilize developing dendrites of starburst amacrines. During the first 2 postnatal weeks, subpopulations of anti-NF-M-labeled ganglion cells costratified with the preexisting dendritic strata of starburst amacrines in the ON sublamina, OFF sublamina, or both. Hence, anti-NF-M-labeled ganglion cells may include direction-selective ones. Thereafter, NF-M and alpha-internexin proteins disappeared from starburst amacrines, and NF-M immunoreactivity was lost in the dendrites of ganglion cells. Our findings suggest that NF-M and alpha-internexin are important for starburst amacrines and ganglion cells to recognize each other and, thus, contribute to the formation of early developing retinal circuits in the inner plexiform layer.

Early development of the nervous system of the eutherian <i>Tupaia belangeri</i>

“…Next we have investigated the development of cholinergic amacrine cells in the retina of Tupaia belangeri (Knabe et al, 2007). Through the optimization of standard immunohistochemistry protocols, cholinergic amacrine cells which play key roles "in originating retinal directional selectivity and optokinetic eye movement" (Yoshida et al, 2001) could be detected 2 weeks earlier than had been reported previously (Sandmann et al, 1997).…”

“…Different from photoreceptor cells in mice and men, the nuclei of these cones are not stacked upon one another, but clearly arranged in only one row. Consequently, both the development of cones and rods (Knabe, 1995;Knabe and Kuhn, 1996a, b, 1997, 1998a and the establishment of the associated neural networks can be studied under particularly favorable conditions (Müller and Peichl, 1991a, b;Engelmann and Peichl, 1996;Sandmann et al, 1997;Knabe et al, 2007). On the other hand, the tree shrew retina is consulted in clinical contexts due to its extensive structural similarity to the primate retina, e.g., for documentation of retinal thinnings following induced high myopia via in vivo optical coherence tomography (Abbott et al, 2009(Abbott et al, , 2011.…”

“…These dendrites provide the scaffold for the dendrites of directionally selective ganglion cells which contact starburst amacrines with a delay (Knabe et al, 2007). Most probably, proper development of these networks depends on the presence of stable neurofilaments resulting from the coexpression of neurofilament protein M (NF-M, 150 kDa) and α-internexin in the dendrites of starburst amacrines (Fig.…”

“…6). As soon as the earliest functional synapses have formed in the inner plexiform layer (Foelix et al, 1987), both the dendrites of starburst amacrine cells and the dendrites of directionally selective ganglion cells downregulate NF-M and/or α-internexin (Knabe et al, 2007). The obvious question to ask here is whether the transient coexpression of these two neurofilament proteins not only stabilizes the dendrites of starburst amacrines and ganglion cells but also somehow promotes their mutual recognition.…”

“…The temporary occurrence of α-internexin during defined developmental periods, as seen in the retina of Tupaia belangeri (Knabe et al, 2007), suggests that α-internexin might play a role in neuroplasticity. Under this premise, Liu et al (2013) have studied the expression patterns of α-internexin in neuronal lineages of the developing chick retina.…”