Axons of Alpha Ganglion Cells Regenerate
Faster Than Other Types Into a Peripheral
Nerve Graft in Adult Cats
Hideki Maki,
1
Masami Watanabe,
2
*
Yoshihito Tokita,
3
Kiyoshi Saito,
1
and Jun Yoshida
1
1
Department of Neurosurgery, Nagoya University School of Medicine, Nagoya, Aichi, Japan
2
Department of Physiology, Institute for Developmental Research, Kasugai, Aichi, Japan
3
Department of Perinatology, Institute for Developmental Research, Kasugai, Aichi, Japan
We reported previously that alpha ganglion cells in the
cat retina have the highest ability in axonal regeneration.
To examine whether alpha cells regenerate axons faster,
we estimated the rate of axonal regeneration of retinal
ganglion cells (RGCs) with transplantation of a peripheral
nerve (PN) segment. After 4, 6, and 8 weeks of survival,
regenerated RGCs were double-labeled with two fluores-
cent dyes injected separately at 10 mm and 20 mm from
the connected site. From a scatter diagram of double-
labeling ratios, we estimated that axons reached 20 mm
by 3.2 weeks. Immunostaining suggested that first axon
sprouts entered a PN segment on Day 4. These values
enabled us to estimate average rates of axonal regener-
ation as 1.1 mm/day for all the RGCs. Proportions of cell
types of regenerated RGCs were obtained with Lucifer
yellow injections, and those of alpha cells were higher
than those in normal retinas in any periods. From analysis
of scatter diagrams, we estimated axonal growth rate
of alpha, beta, and non-alpha/beta cells as 1.4, 1.1,
1.0 mm/day, respectively. The higher regeneration rate of
alpha cells may reflect greater regenerative ability com-
pared to other cell types. The present system also pro-
vides control values when a method to promote axonal
regeneration is developed. © 2003 Wiley-Liss, Inc.
Key words: retinal ganglion cells; axonal regeneration
rate; peripheral nerve transplantation; adult cats
Axons of retinal ganglion cells (RGCs) in adult
mammals regenerate when a segment of peripheral nerve
(PN) is transplanted to the transected end of the optic
nerve (ON) (Aguayo, 1985; So and Aguayo, 1985). We
have been studying ON regeneration in adult cats because
cats have a developed visual system, as primates do, and are
suitable for research on functional recovery of impaired
visual pathways (Watanabe et al., 1991; Watanabe and
Fukuda, 2002). We have revealed some aspects of cat
RGCs with regenerated axons. Regenerated RGCs retain
their morphological and physiological properties even for
60 days after axotomy (Watanabe et al., 1993; Miyoshi et
al., 1999; Watanabe and Fukuda, 2002). Alpha cells have
a greater ability for axonal regeneration than do other cell
types (Watanabe et al., 1993; Miyoshi et al., 1999). Their
higher regenerative ability can be attributed partly to
higher resistance against axotomy; alpha cells survive axo-
tomy better than beta cells for 14 days or longer than 60
days (Holla ¨nder et al., 1985; Silveira et al., 1994; Wa-
tanabe et al., 1995, 2001).
Although cat RGCs regenerate axotomized axons,
fewer than 4% regenerate their axons into a PN graft
(Watanabe et al., 1993), and the numbers are too small to
expect functional recovery of impaired acute vision. It is
reasonable to think that promotion of axotomized RGC
survival results in more regenerated RGCs. In fact, when
the survival of RGCs is raised with an injection of neu-
rotrophic factors and forskolin, an accelerator of adenylate
cyclase, the numbers of regenerated RGCs increase sig-
nificantly (Watanabe et al., 2003); however, axonal regen-
eration of surviving RGCs is not promoted. Moreover,
we observed that most of these surviving RGCs without
regeneration belonged to non-alpha/beta (NAB) cells.
This observation suggested that a method that facilitates
axon elongation should be developed, to promote both
axonal regeneration and survival of axotomized RGCs.
To develop a method facilitating axonal regeneration,
actual regeneration rates of alpha, beta and NAB cells are
required to assess the method.
We examined regeneration rates of axotomized
RGCs with PN transplantation in adult cats. We first
estimated axonal regeneration rate as a whole. The esti-
Contract grant sponsor: Ministry of Education, Culture, Sports, Science and
Technology; Contract grant number: 1169427, 12358016, 12671733;
Contract grant sponsor: Special Coordination Fund for Promoting Science
and Technology.
*Correspondence to: Masami Watanabe, Department of Physiology, Insti-
tute for Developmental Research, Kasugai, Aichi 480-0392, Japan.
E-mail: mwatan@inst-hsc.pref.aichi.jp
Received 18 September 2002; Revised 25 November 2002; Accepted 5
December 2002
Journal of Neuroscience Research 72:218 –226 (2003)
© 2003 Wiley-Liss, Inc.