DEVELOPMENT OF INNERVATION IN TETRAPOD LIMBS
83
on the study of Xenopus laevis (Prestige, 1967) and of
Eleutherodactylus
martinicensis
(Hughes, 1965a).
II. The Anura
A. The Prefunctional Period
The anatomical pattern of the limb nerves is established very early.
The development in the hind limb of Rana pipiens has been described
by Taylor (1943). All the major branches are recognizable at his stage
L5, when the limb bud is less than a millimeter in length, and the
diameter half the length. The same is true of Xenopus laevis at stage 52
of Nieuwkoop and Faber (1956), and in the 5.5-6 day embryo of
Eleutherodactylus
martinicensis
(Hughes, 1965b). In this anuran, limbs
appear as early in ontogeny as in the embryos of higher vertebrates, and
not toward the approach of metamorphosis as in larval Anura.
At these early stages in limb development, the histogenesis of muscles
and of the limb skeleton has not progressed beyond that of the condensation of mesenchyme at the sites of the future major thigh muscles, and of
the more proximal elements of the limb skeleton. In
Eleutherodactylus,
the nerves to the middle digits of the hind limb are recognizable as soon
as their presence is foreshadowed in the outline of the foot, when the
mesenchyme within is still of a uniform density. It is thus clear that the
pattern of the limb nerves is shaped by forces intrinsic to the nervous
system and does not arise secondarily in relation to other structures.
The limb is first penetrated by nerve fibers while it is yet a hemispherical bud. The first nervous elements to enter are naked axons, unaccompanied by Schwann cells, the migration of which along the first bundle of
nerve fibers lags some way behind the forward zone. In
Eleutherodactylus, it seems that the invasive properties of nerve fiber are then
at a maximum. This evidence comes from experiments on the grafting
of limbs that were immediately replaced after amputation (Hughes,
1962). The proportion of such transplants that become innervated
steadily declines with age of operation from early limb bud stages onward, and reaches very low levels after 7 days, when digits are first
visible. It seems that this effect of age is a function of the center and not
of the periphery, for in a further experiment, forelimbs were interchanged
between tw
r
o groups of embryos whose ages w
r
ere 5.5 and 7.25 days,
respectively. Eight days afterward all of the older grafts on younger
hosts had become innervated, whereas with the converse procedure, in no
83
on the study of Xenopus laevis (Prestige, 1967) and of
Eleutherodactylus
martinicensis
(Hughes, 1965a).
II. The Anura
A. The Prefunctional Period
The anatomical pattern of the limb nerves is established very early.
The development in the hind limb of Rana pipiens has been described
by Taylor (1943). All the major branches are recognizable at his stage
L5, when the limb bud is less than a millimeter in length, and the
diameter half the length. The same is true of Xenopus laevis at stage 52
of Nieuwkoop and Faber (1956), and in the 5.5-6 day embryo of
Eleutherodactylus
martinicensis
(Hughes, 1965b). In this anuran, limbs
appear as early in ontogeny as in the embryos of higher vertebrates, and
not toward the approach of metamorphosis as in larval Anura.
At these early stages in limb development, the histogenesis of muscles
and of the limb skeleton has not progressed beyond that of the condensation of mesenchyme at the sites of the future major thigh muscles, and of
the more proximal elements of the limb skeleton. In
Eleutherodactylus,
the nerves to the middle digits of the hind limb are recognizable as soon
as their presence is foreshadowed in the outline of the foot, when the
mesenchyme within is still of a uniform density. It is thus clear that the
pattern of the limb nerves is shaped by forces intrinsic to the nervous
system and does not arise secondarily in relation to other structures.
The limb is first penetrated by nerve fibers while it is yet a hemispherical bud. The first nervous elements to enter are naked axons, unaccompanied by Schwann cells, the migration of which along the first bundle of
nerve fibers lags some way behind the forward zone. In
Eleutherodactylus, it seems that the invasive properties of nerve fiber are then
at a maximum. This evidence comes from experiments on the grafting
of limbs that were immediately replaced after amputation (Hughes,
1962). The proportion of such transplants that become innervated
steadily declines with age of operation from early limb bud stages onward, and reaches very low levels after 7 days, when digits are first
visible. It seems that this effect of age is a function of the center and not
of the periphery, for in a further experiment, forelimbs were interchanged
between tw
r
o groups of embryos whose ages w
r
ere 5.5 and 7.25 days,
respectively. Eight days afterward all of the older grafts on younger
hosts had become innervated, whereas with the converse procedure, in no