238 Brain Research, 279 (1983) 238-240
Elsevier
Regeneration of locomotor command systems in the sea lamprey
SCOTT N. CURRIE and JOSEPH AYERS
Department of Biology and Marine Science Center, Northeastern University, East Point, Nahant, MA O1908 ( U. S. A. )
(Accepted August 2nd, 1983)
Key words: spinal cord - - regeneration - - command neurons - - lamprey
Ammocoete larvae of the sea lamprey were allowed to recover from a complete transection of the spinal cord posterior to the last
gill arch. Specimens were then prepared for focal extracellular stimulation of the brainstem in the region known to contain the com-
mand systems for swimming. In 4 preparations where behavioral recovery had occurred, stimulation in this region would initiate swim-
ming, indicating that the command function of this 'locomotor' region had recovered.
The sea lamprey, a primitive vertebrate, can re-
cover several behaviors following lesions as severe as
complete transection of the spinal cord 1,2,10,19,22,24,2L
Coordinated swimming behavior, for example, can
recover in 50 days 2. Giant brainstem reticulospinal
interneurons have been demonstrated to regenerate
across a spinal transection and form synaptic con-
tacts23-25. Thus the lamprey cord has the capacity for
true regeneration 9, but it has not been established
which neuronal systems are responsible for the re-
covery of any behavior20.
Locomotor movements can be initiated in most
vertebrates by stimulation of command systems I3 in a
brainstem or midbrain 'locomotor' regionS, 6.8,t1.t2.
These 'locomotor' or command regions are physio-
logical concepts and the evoked behavior could be
due to the activation of cell bodies in the stimulated
region or of tracts of axons which pass through the
stimulus site6. The existence of such a command sys-
tem has been recently demonstrated in the lamprey
by extracellular stimulation of a 'locomotor' region in
the bulbar level of the fourth ventricle 4,7,a5.16. In this
report, we will show that cyclic swimming
movements can also be initiated by stimulation of this
command system in specimens which have recovered
from complete spinal cord transection.
Ammocoete larvae (8-12 cm) of the sea lamprey,
Petromyzon marinus were used in all experiments.
Complete spinal cord transection was achieved by
exposing the cord dorsally with a midline incision ex-
tending from the 7th to the llth segment posterior to
the last gill arch. The edges of the incision were re-
tracted laterally and the incision deepened to expose
the und6rlying cord. Transection was achieved by
severing the cord at the level of the 9th segment with
iridectomy scissors or a scalpel. Confirmation of a
complete transection was achieved by lifting the re-
tracted cut ends of the cord to observe the underly-
ing notocord. Lesioned specimens were maintained
as identified individuals in shallow chambers at room
temperature until recovery was complete.
Acutely transected individuals (Stage 1) produced
only rapid head movements with no active undula-
tions of the body caudal to the transection. Recovery
was scored weekly for achievement of several behav-
ioral criteria 2, including production of isolated caudal
flexion waves (stage 2), production of repetitive cau-
dal flexion waves (stage 3), coordination of
movements anterior and posterior to the lesion
(stage 4) and ability to orient relative to gravity
(stage 5). Swimming movements gradually pro-
gressed toward normalcy from stage 3 where they
were quite weak, through stage 5 and were consid-
ered recovered when advancement to stage 5 had oc-
curred.
Recovered stage 5 specimens were placed under
tricaine anesthesia, and prepared for brainstem stim-
ulation by a ventral longitudinal incision through the
gill chamber, which allowed the specimen to be
pinned out by the gill arches (Fig. 1). Iridectomy scis-
0006-8993/83/$03.00 © 1983 Elsevier Science Publishers B.V.