Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden
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ABSTRACT |
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Fagerstedt, Patriq and Fredrik Ullén. Lateral Turns in the Lamprey. I. Patterns of Motoneuron Activity. J. Neurophysiol. 86: 2246-2256, 2001. The activity of motoneurons during lateral turns was studied in a lower vertebrate, the lamprey, to investigate how a supraspinal command for the change of direction during locomotion is transmitted from the brain stem and integrated with the activity of the spinal locomotor pattern generator. Three types of experiments were performed. 1) The muscular activity during lateral turns in freely swimming adult lampreys was recorded by electromyography (EMG). It was characterized by increased cycle duration and increased duration, intensity, and cycle proportion of the bursts on the side toward which the animal turns. 2) Electrical stimulation of the skin on one side of the head in a head-spinal cord preparation of the lamprey during fictive locomotion elicited asymmetric ventral root burst activity with similar characteristics as observed in the EMG of intact lampreys during lateral turns. The cycle duration and ventral root burst intensity, duration, and cycle proportion on the side of the spinal cord contralateral to the stimulus were increased; hence a fictive lateral turn away from the stimulus could be produced. The fictive turn propagated caudally with decreasing amplitude. The increase in burst duration during the turn correlated well with the increase in cycle duration, while changes in contralateral burst intensity and burst duration did not co-vary. Turning responses varied depending on the timing (phase) of the skin stimulation: stimuli in the first two-thirds of a cycle evoked a turn in the same cycle, whereas stimuli in the last third gave a turn in the following cycle. The largest turns were evoked by stimuli in the first third of a cycle. 3) Fictive turns were abolished after transection of the trigeminal nerve or a rhombencephalic midline split, but not in a rhombencephalic preparation with transected cerebellar commissure. High spinal hemisection was sufficient to block turning toward the lesioned side, while turns toward the intact side remained. Taken together these findings suggest that the reticulospinal turn command is essentially unilateral and generated in the rhombencephalon.
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INTRODUCTION |
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Locomotion allows an animal to
move around in its environment to search for food, to find a mate, or
to escape predators. Spinal circuits generate the basic locomotor
movements while supraspinal centers adapt these to the needs and goals
of the animal by sending commands for alterations in speed, postural
corrections, and steering (Grillner 1981;
Orlovsky et al. 1999
).
Lampreys, like elasmobranchs and teleosts, swim forward by propagating
waves of lateral flexion rostrocaudally along their bodies (Gray
1933a; Grillner 1974
; Grillner and Kashin
1976
; Wallén and Williams 1984
). During
turns in the horizontal plane (lateral turns) the muscular activity on
the turning side increases, producing a larger force against the water
on that side, and thus a turn toward the activated side (Gray
1933b
; McClellan and Hagevik 1997
). Neural
correlates of locomotion (fictive swimming) can be elicited in the
lamprey in the brain stem-spinal cord preparation by bath application
of excitatory amino acids to the spinal cord or by electrical or
chemical stimulation of the brain stem (Cohen and Wallén
1980
; Grillner and Wallén 1980
;
McClellan and Grillner 1984
; McClellan and
Hagevik 1997
; Poon 1980
; Wallén and
Williams 1984
). In intact lampreys, mechanical or electrical
stimulation to the skin of the head evokes lateral turns away from the
stimulus (McClellan 1984
). In brain stem-spinal cord
preparations of adult lamprey, the same stimuli evoke an asymmetric
ventral root burst pattern followed by brief episodes of swimming
activity (McClellan 1984
). In the head-spinal cord
preparation of the larval lamprey, fictive locomotion was elicited by
stimulation of the brain stem. On this background electrical
stimulation of the skin on one side of the head elicited modifications
of ventral root burst activity with changes in timing and intensity of
the burst resembling in vivo turns (McClellan and Hagevik
1997
).
Skin stimulation activates trigeminal sensory afferents
(McClellan 1984), which in turn evoke excitatory and
inhibitory postsynaptic potentials (EPSPs and IPSPs, respectively) in
ipsi- and contralateral reticulospinal (RS) neurons (Rovainen
1967
; Viana Di Prisco et al. 1995
;
Wickelgren 1977
). RS neurons constitute the main
descending system in the lamprey (Bussières 1994
;
Ronan 1989
; Rovainen 1967
, 1974
; Swain et al. 1993
). They activate
ipsilateral motoneurons directly and also influence bilateral motor
output indirectly through the segmental spinal networks
(Buchanan 1982
; Ohta and Grillner 1989
;
Rovainen 1974
). There are also crossing excitatory connections from the brain stem to spinal cord segments (e.g., from
Mauthner cells) (Rovainen 1974
).
Here we describe the activity of motoneurons during lateral turns and
in the accompanying paper (Fagerstedt et al. 2001) the corresponding supraspinal commands. Three sets of experiments were
performed in this study. First, we investigated the EMG pattern of the
turn in freely swimming lamprey. Second, we have developed a
head-spinal cord preparation of the adult lamprey, in which turn-like
asymmetric ventral root activity (fictive lateral turns) could be
elicited by skin stimulation. By using this preparation, we examined
the relationships between the turn characteristics and the phase of
skin stimulation in the locomotor cycle. Third, the course of
descending pathways responsible for elicitation of turns was
investigated in lesion experiments. Preliminary accounts of these
results have appeared in abstract form (Fagerstedt et al.
1998
; Ullén et al. 1998
).
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METHODS |
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Animals
Adult river lampreys (Lampetra fluviatilis, 20-30 cm total length, n = 7) were used in in vivo experiments, and American silver lampreys (Ichthyomyzon unicuspis, 15-25 cm total length, n = 30) were used in in vitro experiments. They were obtained from commercial suppliers in Sweden and Iowa, respectively. Animals were kept in aerated fresh water aquaria at 5°C in 12 h light/12 h darkness until used.
Surgical procedures
Animals were anesthetized by immersion in cold water containing tricaine methane sulfonate (MS-222, Sigma; 200 mg/l water) adjusted to pH 7.4. Insertion of electromyographic (EMG) electrodes for the in vivo experiments was performed in a chamber with a mixture of anesthetic and fresh water. Bipolar EMG electrodes were made from a wire with two insulated, stainless steel leads, 100 µm in diameter. The wire was threaded through the barrel of a 22-gauge hypodermic needle. The tips (0.5 mm) of the wires were stripped of insulation, and spread 0.5-1.0 mm apart and bent into a hook, which was then pulled back and nestled into the tip of the barrel of the needle. Using these needles, EMG electrodes were implanted in the muscle bilaterally, caudal to the last gill, and immediately rostral to the anterior dorsal fin. The cables from all four electrodes were wired together to form one bundle originating at the start of the dorsal fin. The animal was then transferred to the experimental aquarium containing fresh water, until it recovered from the anesthesia. All surgical procedures were performed according to principles of laboratory animal care, as approved by the Swedish National Board for Laboratory Animals-CFN (LSFS 1988:45), Swedish law (SFS 1988:534/539/541), and the European Communities Council (directive 86/609/EEC). The experiments were approved by Stockholms Norra Djurförsöksetiska Nämnd.
For in vitro experiments the head and the rostral half of the spinal
cord with the underlying notochord, usually 20-50 segments long, were
dissected in cold oxygenated saline of the following composition (in
mM): 91 NaCl, 2.1 KCl, 2.6 CaCl2, 1.8 MgCl2, 20 NaHCO3, 0.5 L-glutamine, and 4 glucose, buffered to pH 7.4 by bubbling
with 95% O2-5% CO2
(Wickelgren 1977). The preparation was pinned down in a
silicone elastomer (Sylgard, Dow Corning, Midland, MI)-lined cooling
chamber (8-12°C) perfused with the cold oxygenated saline. A plastic
barrier at segment 2-6, sealed with agar, was used to divide the
chamber into a brain and a spinal cord pool (Fig.
1B).
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Swimming trials
Turns in intact animals were recorded in a shallow (8 cm deep) L-shaped aquarium with a white fluorescent lamp positioned along one of the walls as illustrated in Fig. 1A. The water temperature in the aquarium was 7-10°C. The behavior of the animals was recorded with a video camera (25 frames/s), and the locomotor activity was recorded with EMG electrodes (see above).
After being transferred to the aquarium, the animals spontaneously
assumed a quiescent position, attached to the bottom of the aquarium
with their sucker mouth. As a rule, the passive animals could be moved
gently with the hand to the indicated starting position (marked by an
asterisk in Fig. 1A). Locomotion was evoked by illuminating
the tail of the animals, which contains dermal photoreceptors
(Ullén et al. 1993; Young 1935
),
with an optical guide (8 mm diam, 90 W white lamp) held 1-2 cm away.
As the animals swam along the illuminated side of the aquarium, they
typically performed a lateral turning movement away from the light
(negative phototaxis).
In vitro experiments
Fictive locomotion was induced by addition of D-glutamate (0.5-2 mM; Tocris Cookson, Bristol, UK) to the oxygenated saline in the spinal cord pool (Fig. 1B). Locomotor activity was recorded from a pair of rostral (segments 10-20) and caudal (segments 20-35) ventral roots by gently pressing the tips of Ringer solution-filled glass electrodes against the roots. Two additional electrodes were used to record activity from the surface of the caudal end of the spinal cord (usually segments 35-50). Asymmetric ventral root activity was evoked by DC electrical stimulation (train of 2-ms pulses, 10-50 Hz, 250-1,500 ms duration) of the skin to one side of the head by bipolar silver wires (0.5 mm diam), insulated except for the tips. Due to variability in excitability between preparations and adaptation of the stimulated skin, the current strength (10-1,000 µA) was varied between trials. Recordings were digitized on-line (sampling period 480-1,000 µs) using Axoscope 7 software and a Digidata 1200 A/D board (Axon Instruments, Foster City, CA).
Data processing and analysis
Each video record of a swimming lamprey was first analyzed qualitatively, and trials with turning movements were selected. The video records were analyzed frame by frame, and the interval during which a turn occurred was indicated on the EMG record. The time of onset and termination of EMG and ventral root bursts were detected by a semi-automatic selection algorithm (Datapac 2000; Run Technologies, Laguna Hills, CA). Onset and termination points were used to calculate burst duration and cycle duration (BD and CD in Fig. 1C). Burst proportion was calculated as the ratio between burst duration and cycle duration. Burst intensity was calculated as burst amplitude, defined as the area of the rectified burst, divided by burst duration. The delay/overlap between ventral root bursts was calculated for in vitro turns only and labeled interburst duration 1 and 2 (IB1 and IB2 in Fig. 1C).
The cycles containing the maximum body curvature in the in vivo
records, and the onset of the stimulus train in the in vitro records,
respectively, were labeled cycle 0. The five cycles before (5 to
1)
and after (1 to 5) cycle 0 were analyzed for each stimulus train. All
parameters were normalized against the mean value of that of the cycles
preceding cycle 0. All statistical analyses used ANOVA
(* P < 0.05 and ** P < 0.01).
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RESULTS |
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In vivo turns
When a swimming lamprey approached the illuminated area of the aquarium, it turned away from the light (Fig. 1A). Figure 2A shows the EMG activity during a turn to the left (the turning side). The burst of left rostral EMG activity just preceding the point of maximum body curvature (defining cycle 0) is increased in duration leading to an increased cycle duration. This was followed by an increased burst duration and intensity on the nonturning side, here termed rebound, further increasing the cycle duration.
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Averaging 14 turns from 7 animals around the point of maximum body curvature showed an increased cycle duration during turns (Fig. 2B), which usually began with a burst on the turning side. The duration and intensity of this burst was increased (Fig. 2, C and E). In some experiments (cf. Fig. 2A) it was followed by an increased burst duration and intensity on the opposite side, but no significant increase of the mean could be observed. The burst proportion on the turning side was increased, while the burst proportion on the opposite side was decreased, except in cases with a rebound, where it could be unchanged or increased instead (Fig. 2D). All turn-related changes in burst intensity and duration were larger in the rostral segments compared with the caudal ones (data not shown).
In vitro turns
A brain-spinal cord preparation was placed in a two-pool experimental chamber (Fig. 1B), where rhythmic symmetric left-right alternating ventral root activity (fictive locomotion) was induced by bath application of D-glutamate (see METHODS). Short trains of electrical impulses (see METHODS) to the skin on the left side of the head (L skin stim) evoked a transient asymmetry in the ventral root bursting pattern (Fig. 3A). The first ventral root bursts on the contralateral side to the stimulus (R rostr VR and R caud VR) after the beginning of the stimulus train were prolonged and increased in intensity. The contralateral response was followed by larger and longer-than-normal ipsilateral bursts (L rostr VR and L caud VR in Fig. 3A). Stimulation of the skin on the right side of the head modulated the ventral root output in the opposite way (Fig. 3B). Ventral root responses were associated with a bilateral increase of activity recorded from the surface of the caudal part of the spinal cord (data not shown). There was no significant difference in the amplitude of the wave on the two sides, and the latency of the wave corresponded to a minimum conduction velocity of 3 m/s of a putative descending pathway.
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A quantitative analysis performed on ventral root responses to skin stimulation (n = 195) in seven animals is shown in Fig. 4. Duty cycles were defined as starting with the onset of a ventral root burst ipsilateral to the stimulated side, and cycle 0 was defined as the cycle in which the stimulus train began (see Fig. 1C). With this procedure the response never occurred earlier than cycle 0. All responses to stimulation were further divided into three groups in Fig. 5 depending on whether the onset of the stimulation occurred during the ipsilateral burst (phase 1), or during the first or second half of the contralateral burst (phases 2 and 3, respectively; see Fig. 1C). The mean duration of cycle 0 was prolonged (Fig. 4A). The increase was mainly due to an increase in burst duration on the side contralateral to skin stimulation (Fig. 4B). The preceding ipsilateral burst was slightly prolonged or unchanged depending on whether the stimulation started early or late in cycle 0 (Fig. 5B). The interval between the contralateral burst of cycle 0 and ipsilateral burst of cycle 1 was shortened (IB2 in Fig. 4C). Cycle 1 was also prolonged (Fig. 4A), and began with a longer-than-normal ipsilateral burst (Fig. 4B) followed by a contralateral burst, the length of which was also dependent on stimulus phase (Fig. 5B). Consequently, the burst proportion was increased on the contralateral side and decreased on the ipsilateral side in cycle 0 (Fig. 4D). The burst intensity (Fig. 4E) was increased on both sides, but the increase was significantly larger on the side contralateral to the stimulus. The ipsilateral burst proportion and intensity was also increased during cycle 1, while the contralateral one remained unchanged (Fig. 4, D and E). The phase analysis showed that stimulus trains beginning in phase 1 and 2 increased the cycle duration in the cycles 0 and 1 (Fig. 5A), the contralateral burst duration, proportion, and intensity in cycle 0 (Fig. 5B), and the ipsilateral burst duration in cycle 1 (Fig. 5C). Stimulation trains given early in the swim cycle (in phase 1), also produced a marked increase in the ipsilateral burst intensity in cycle 0 (Fig. 5E). Stimulation later in the cycle, that is after the midpoint of the contralateral burst (phase 3) had its main effect on cycle duration and burst duration and intensity delayed by one cycle, occurring in cycle 1 rather than in cycle 0.
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All changes in the rostral segments were mirrored in more caudal
segments, although with a smaller amplitude (Figs. 3, A and B, and 4, A-E). Turn-like changes in both rhythm
and burst intensity could be observed down to the 50th segment but was
less clear or absent further caudally (one preparation, tested to
segment 70). These transient changes in fictive locomotor activity
resemble the asymmetric muscle activity observed in the intact adult
(see Fig. 2) (McClellan 1984) and in larval lampreys
during in vivo turns (McClellan and Hagevik 1997
), and
the response is thus by us labeled "fictive turn."
The amplitude of the ventral root response to skin stimulation differed between trials and between preparations (data not shown). The increase in cycle duration in cycle 0 correlated positively with an increase in burst duration on the contralateral side (R2 = 0.2352, n = 195 in 7 preparations; Fig. 6A), the normalized burst duration increasing around twice as much as the normalized cycle duration. In some preparations, different stimuli could produce either a strong increase in burst duration on the contralateral side, or a strong increase in the burst intensity without a proportional increase in the burst duration, suggesting that these two characteristics may vary independently (R2 = 0.0002, n = 82; Fig. 6B).
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Pathway for the lateral turn command
The pathway for fictive turns evoked by skin stimulation was
investigated by transecting different cranial nerves on the stimulated side and by making lesions in the brain stem and spinal cord (Fig. 7, A and E). The
skin stimulus was transmitted to the brain stem in trigeminal afferents
since transection of the trigeminal (lesion 4 in Fig.
7E; not illustrated), but no other cranial nerve on the
stimulated side abolished fictive turns (n = 3) (see
also McClellan 1984). Rhombencephalic midline lesions
(lesion 5 in Fig. 7E) also blocked the fictive
turns (n = 4, data not shown) demonstrating that the
signals need to cross the midline at the rhombencephalic level. In
these preparations, skin stimulation occasionally caused increased
ipsilateral activation of the ventral roots. Fictive turns could be
evoked in rhombencephalic preparations [transection of the brain stem
at the rostral border of the rhombencephalon (lesion 1 in
Fig. 7A), n = 6; Fig. 7B],
showing that pathways through mesencephalon are not necessary to
generate turning responses. Similarly, a section of the cerebellar and
posttectal commissures (lesion 2 in Fig. 7A) did
not affect fictive turning (n = 4; Fig. 7C).
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To elucidate the role of ipsilateral and contralateral components of the descending commands at the spinal level, hemisections of the rostral spinal cord (segments 1-6) were performed either on the side ipsilateral (lesion 3 in Fig. 7A) or contralateral to the stimulated side (lesion 6 in Fig. 7E). Hemisections ipsilateral to the stimulated side did not abolish fictive turns (n = 3; Fig. 7D). The cycle duration (Fig. 8A), the contralateral burst duration (Fig. 8B), and intensity (Fig. 8C) were increased during cycle 0. On the side ipsilateral to the stimulated skin, there was no increase in the mean burst duration (rebound) during cycle 1 after the ipsilateral lesion (Fig. 8B), although rebounds were observed in a few experiments. The descending wave of activity recorded from the surface of the caudal spinal cord was practically abolished on the lesioned side (data not shown) indicating that most of this activity originated above the lesion (i.e., in the brain stem). A hemisection of the spinal cord on the side contralateral to the stimulation blocked the generation of turns (n = 3; Fig. 7F). No increase in contralateral burst duration, or in the cycle duration could be observed during cycle 0 (Fig. 8, D and E). The increase in burst duration on the ipsilateral side during the following cycle (rebound) was also absent (Fig. 8E). There was still, however, an increase in the burst intensity on the contralateral side, albeit smaller than in the control, while on the ipsilateral side the increase in burst intensity was greater than normal, especially during cycle 1 (Fig. 8F).
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In five preparations, spinal hemisections were performed at a level between the rostral and caudal pair of the recorded ventral roots. The propagation of the turn was undisturbed by lesion on the side ipsilateral to the stimulus, suggesting that local interactions between the two sides of the spinal cord are not a necessary part of the descending turn command (data not shown). Lesions on the contralateral side blocked the fictive turn in more caudal segments, demonstrating that a perturbation of the alternating ventral root bursting pattern in the form of fictive turn does not traverse a spinal hemisection (data not shown). These results suggest that axons running in the spinal cord contralateral to the stimulus are necessary for transmitting the turn command caudally.
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DISCUSSION |
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In the present study we utilize the possibility of eliciting
asymmetric spinal motor activity by electrical skin stimulation to one
side of the head, first demonstrated by McClellan and co-workers (McClellan 1984; McClellan and Hagevik
1997
), to investigate the descending pathways and phase
dependence of descending commands for lateral turns in the adult
lamprey. We have shown that the EMGs underlying lateral turns in freely
swimming adult lampreys are characterized by an increased cycle
duration during the turn, as well as an increased burst duration, burst
proportion, and burst intensity on the side of the turn (Fig. 2). These
changes in muscular activity are similar to those observed during
lateral turns in intact larval lampreys (McClellan and Hagevik
1997
), thus indicating that the motor pattern for lateral
turning is conserved during metamorphosis from the larval to the adult
stage, and is similar to that of teleosts (Gray 1933b
).
Fictive turns evoked by electrical skin stimulus
Brief electrical skin stimulation to one side of the head of adult lamprey brain-spinal cord preparations during fictive locomotion evoked a transient asymmetry in the alternating ventral root burst activity. The changes in ventral root activity included an increased cycle period with increased burst duration, burst proportion and intensity on the side contralateral to the stimulus, followed by an increased burst duration and proportion on the ipsilateral side (rebound; Figs. 3 and 4). The largest responses were observed in the rostral segments of the spinal cord, then decreasing in size caudally, and present at least down to the 50th segment.
This asymmetric motor output, here labeled fictive turn, is very
similar to the changes in EMG activity recorded during lateral turns
and would thus direct the body of the lamprey away from the skin
stimulus (present study and McClellan 1984). The rebound was less evident during in vivo turns, but was observed in some experiments (cf. Fig. 2A, and in intact larval lampreys)
(McClellan and Hagevik 1997
). Similar responses to
electrical skin stimulation were also observed in the larval lamprey in
vitro (McClellan and Hagevik 1997
) where fictive
locomotion was induced by chemical microstimulation of the brain stem.
Both these in vitro studies show that it is possible to modulate the
spinal locomotor central pattern generator (CPG) to transiently switch
from symmetric activity ("rectilinear swimming") to an asymmetric
activity ("turning" away from a stimulus), i.e., that fictive turns
can be generated without sensory feedback from the movement performed.
Lateral turns are characterized by changes both in timing (cycle duration, burst duration) and in intensity of the locomotor bursts. We found that electrical skin stimulation could evoke both responses with large increases in burst intensity combined with a small prolongation of the burst duration, as well as responses with small burst intensity increases coupled to a large increase in burst duration (Fig. 6B). This suggests that certain turn characteristics can vary independently of each other. Whether different turn strategies are used in different behavioral contexts remains to be investigated.
Pathway of the descending turn command
Neither transection of the brain stem rostral to the
rhombencephalon, nor a transection of the cerebellar commissure
affected fictive turns elicited from a trigeminal stimulus (Fig. 7,
A-C). A hemisection of the spinal cord on the same side as
the stimulus also failed to block the descending turn command (Fig.
7D). Fictive turns were significantly attenuated, however,
by a contralateral hemisection of the spinal cord (Fig. 7, E
and F), showing that the pathway for fictive turns crosses
over to the contralateral side in the rhombencephalon. This was
verified by a performing a midline split of the rhombencephalon, which
abolished fictive turns. Lesions of the ipsilateral trigeminal nerve,
but not sectioning of any other cranial nerve, also blocked the
response, showing that the turning response is dependent on trigeminal
afferent pathways. Previously it was shown that trigeminal afferents
activated by skin stimulation of the head, both can initiate locomotion and elicit avoidance responses, through activation of descending pathways originating in the brain stem (McClellan 1984;
McClellan and Grillner 1983
). Trigeminal afferents
originate from dorsal cells in the medulla and rostral spinal cord and
the trigeminal ganglia where the central projections terminate in the
sensory part of the ipsilateral trigeminal nucleus (Koyama et
al. 1987
; Matthews and Wickelgren 1978
). They
synapse on excitatory and inhibitory relay neurons, some of which have
ipsilateral descending projections to the spinal cord (Ronan
1989
). Trigeminal nerve stimulation evokes polysynaptic mixed
IPSP-EPSPs in both ipsilateral and contralateral reticular nuclei
(Rovainen 1967
; Viana Di Prisco et al.
1995
; Wickelgren 1977
). The fact that turns
could be generated in rhombencephalic preparations shows that these
bilateral trigemino-reticular pathways are likely to carry the signals
eliciting a turn (Fig. 7).
The RS system is the main descending system in the lamprey and is
composed of hundreds of mainly ipsilaterally projecting neurons in four
bilateral reticular nuclei, and also the Mauthner and accessory
Mauthner neurons, which project to the contralateral spinal cord
(Bussières 1994; Nieuwenhuys and Nicholson
1998
; Swain et al. 1993
). Our results further
demonstrate that unilateral pathways at the level of the spinal cord,
running on the side contralateral to the stimulus, are both necessary
and sufficient for transmitting the descending turn command. Spinal
hemisections ipsilateral to the stimulated side between the two pairs
of ventral root electrodes did not block the propagation of the turn
caudally, revealing that the descending turn command is not dependent
on local interactions between the left and right subdivisions of the
spinal CPG. The rebound could partly be caused by descending commands
on the side ipsilateral to the stimulus since it was attenuated after
high ipsilateral spinal hemisections (Figs. 7 and 8). Spiking activity
of reticulospinal neurons on the ipsilateral side during the rebound
was also seen occasionally (see Fagerstedt et al. 2001
).
It is not clear, however, whether it is part of the descending turn
command or a spinal rebound mechanism since a similar phenomenon was
observed after stimulation of long axons in the contralateral half of
the isolated lamprey spinal cord (Rovainen 1985
). The
function of the rebound activity during turning behavior is unclear,
but it has been speculated that it could serve as restoring force after
the turn (McClellan and Hagevik 1997
).
Phase dependence of fictive turns
Voluntary movements, ongoing activity, and evoked reflexes can be in conflict with each other and must either be integrated, or the conflict must be resolved at some level in the control hierarchy (i.e., motoneurons, the CPG, or the level of descending command neurons). In vivo, feedback from ongoing locomotor activity is presumably also important to integrate the turn with locomotion, by switching behavior in the optimal phase of the movement, and with the correct amplitude and direction.
We have shown that the changes in the characteristics of a fictive turn
depended on in which phase of the swim cycle the stimulus was given
(Fig. 5). This dependency on the phase of stimulus could arise at
several levels of the lamprey CNS. The skin stimulus is first relayed
to the trigeminal nucleus. Trigeminal neurons may receive phasic
information from the spinal cord (Dubuc et al. 1993;
Vinay et al. 1998a
,b
), which could modulate the
transmission of the turn command. The reticulospinal neurons in the
different reticular nuclei receive phasic ascending signals from the
locomotor networks in the most rostral spinal cord during fictive
locomotion (Dubuc and Grillner 1989
; Kasicki and
Grillner 1986
; Kasicki et al. 1989
). In this
preparation, however, where the agar barrier is located over segments
2-6, intracellular recordings from these cells indicate that the
amplitude of the phasic modulation is low (Fagerstedt et al.
2001
).
Phasic dependence on stimulation could also arise in the spinal cord.
The different locomotor interneurons and motoneurons are rhythmically
modulated during locomotion (Buchanan and Cohen 1982;
Buchanan and Kasicki 1995
; Buchanan et al.
1989
). A descending command would have a greater effect if it
arrives when the neurons are in their depolarized phase (on the active
side of locomotor network), than if they occur on the inactive,
hyperpolarized side.
Integration of the descending turn command
To change behavior from rectilinear swimming to horizontal
turning, either separate mechanisms in the spinal cord should be activated, or the activity of the neuronal networks controlling rectilinear swimming should be modified. Changes in the activity of
motoneurons could be caused either by a direct effect on motoneurons exerted by descending pathways, or indirectly, by affecting the locomotor interneurons, or by a combination of both. The changes in
cycle duration and burst duration, however, require modulation of the
activity of locomotor interneurons, i.e., the CPG. RS neurons have been
shown to monosynaptically excite both spinal motoneurons and
interneurons constituting the locomotor CPG (Ohta and Grillner 1989). The lamprey locomotor CPG can be modeled as two
hemi-segments coupled by reciprocal inhibition (Buchanan
1986
; Buchanan and Grillner 1987
). Results from
computer modeling studies indicate that excitation by descending
pathways of the crossing inhibitory interneurons plays an important
role for the increase of cycle and burst duration during turning
(Kozlov et al. 2001
).
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ACKNOWLEDGMENTS |
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We thank S. Grillner, G. N. Orlovsky, and D. Parker for valuable comments on the manuscript.
Support by grants from the Swedish Medical Research Council (MFR 3026), the Swedish Research Council for Engineering Sciences (TFR 282-96-905), Karolinska Institutet, Åke Wibergs Stiftelse, Magnus Bergwalls Stiftelse, and the Swedish Brain Foundation is gratefully acknowledged.
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FOOTNOTES |
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Present address and address for reprint requests: F. Ullén, Neuropediatrics, Dept. of Woman and Child Health, Astrid Lindgren Children's Hospital, SE-171 76 Stockholm, Sweden (E-mail: Fredrik.Ullen{at}neuro.ki.se).
Received 21 June 2000; accepted in final form 11 June 2001.
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REFERENCES |
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