Localization of Choline
Acetyltransferase in the Developing and
Adult Turtle Retinas
LYNETTE T. NGUYEN,
1
JOAQUIN DE JUAN,
2
MARIA MEJIA,
1
AND
NORBERTO M. GRZYWACZ
1
*
1
The Smith-Kettlewell Eye Research Institute, San Francisco, California 94115
2
Departamento de Biotecnologı ´a, Facultad de Ciencias, Universidad de Alicante,
03080 Alicante, Spain
ABSTRACT
Acetylcholine has important epigenetic roles in the developing retina. In this study, cells
that expressed choline acetyltransferase (ChAT), the enzyme that synthesizes acetylcholine,
were investigated in embryonic, postnatal, and adult turtle retinas by using immunofluores-
cence histochemistry. ChAT was present at stage 15 (S15) in cells near the vitreal surface.
With the formation of the inner plexiform layer (IPL) at S18, ChAT-immunoreactive (-IR)
cells were located in the inner nuclear layer (INL) and the ganglion cell layer (GCL). In the
INL, presumed starburst amacrine cells were homogenous in appearance and formed a single
row next to the IPL: This pattern was conserved until adulthood. In the GCL, however, there
were multiple rows of ChAT-IR cells early in development, and this high density of labeled
cells continued during the embryonic stages, until around birth. The high density of ChAT-IR
cells in the GCL was due in part to a population of cells that expressed ChAT transiently. In
postnatal stages and adult retinas, the presumed starburst amacrine ChAT-IR cells formed
two mirror-like rows of homogenous cells on both borders of the IPL. Two cholinergic
dendritic strata that were continuous with these cells were observed as early as S18, and
their depths in the IPL were relatively stable throughout development. A third population of
ChAT-IR cells was observed toward the middle of the INL around S25 and persisted into
adulthood. Finally, cells in the outer nuclear layer (ONL) were ChAT-IR during the embry-
onic stages, were less immunoreactive during the postnatal stages, and were not immuno-
reactive in the adult retinas. J. Comp. Neurol. 420:512–526, 2000. © 2000 Wiley-Liss, Inc.
Indexing terms: amacrine cells; choline acetyltransferase; cell density; development; fluorescence
microscopy; immunohistochemistry, photoreceptor cells; retinal ganglion cells;
starburst amacrine cells; transient population; turtles; vertebrates
A small population of amacrine cells in the adult verte-
brate retina synthesizes acetylcholine (Masland and Liv-
ingstone, 1976; Masland and Mills, 1979) and releases
acetylcholine (Masland and Livingstone, 1976; Masland
and Mills, 1979; Massey and Redburn, 1982). To date,
cholinergic amacrine cells have been identified in neonatal
and adult vertebrates, including human (Hutchins and
Hollyfield, 1987), monkey (Mariani and Hersh, 1988), cat
(Schmidt et al., 1985; Pourcho and Osman, 1986; Dann,
1989), rat (Voigt, 1986), pig (Eckenstein and Thoenen,
1982), rabbit (Masland and Mills, 1979; Masland et al.,
1984), tree shrew (Conley et al., 1986; Sandman et al.,
1997), chicken (Millar et al., 1985, 1987), dogfish (Bran-
don, 1991), goldfish (Famiglietti and Tumosa, 1987), and
turtle (Criswell and Brandon, 1992; Guiloff and Kolb,
1992). These cells make direct connections to ganglion
cells (Famiglietti, 1983b) and, thus, directly shape how
visual stimuli are processed. In the adult retina, these
cholinergic cells are synonymous with the well-described
starburst amacrine cells (Famiglietti, 1983a; Vaney, 1984;
Tauchi and Masland, 1984), which have a role in direc-
tional selectivity (Ariel and Daw, 1982; Vaney, 1990;
Grant sponsor: National Eye Institute: Grant numbers: EY08921 and
EY11170; Grant sponsor: DGICYT; Grant number: PB-96-0414.
*Correspondence to: Dr. Norberto M. Grzywacz, The Smith-Kettlewell
Eye Research Institute, 2318 Fillmore Street, San Francisco, CA 94115.
E-mail: nmg@ski.org
Received 30 March 1999; Revised 13 January 2000; Accepted 13 January
2000
THE JOURNAL OF COMPARATIVE NEUROLOGY 420:512–526 (2000)
© 2000 WILEY-LISS, INC.