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Division of Biological Science, University of Missouri, Columbia, Missouri 65211
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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McClellan, Andrew D. and André Hagevik. Descending control of turning locomotor activity in larval lamprey: neurophysiology and computer modeling. J. Neurophysiol. 78: 214-228, 1997. The purpose of the present study was to examine the mechanisms that produce natural spontaneous turning maneuvers in larval lamprey. During swimming, spontaneous turning movements began with a larger-than-normal bending of the head to one side. Subsequently, undulations propagated down the body with greater amplitude on the side ipsilateral to the turn. During turning to one side, which usually occurred within one cycle, the amplitude and duration of ipsilateral muscle burst activity as well as overall cycle time increased significantly with increasing turn angle. In in vitro brain/spinal cord preparations, brief electrical stimulation applied to the left side of the oral hood at the onset of locomotor burst activity on the right side of the spinal cord produced turninglike motor activity. During the perturbed cycle, the duration and amplitude of the burst on the right as well as cycle time were significantly larger than during preceding control cycles. In several lower vertebrates, unilateral stimulation in brain stem locomotor regions elicits asymmetric, turninglike locomotor activity. In the lamprey, unilateral chemical microstimulation in brain stem locomotor regions elicited continuous asymmetric locomotor activity, but there was little change in cycle time, as occurs during the single turning cycles in whole animals. The descending mechanisms responsible for producing turning locomotor activity were examined with the use of a computer model consisting of left and right phase oscillators in the spinal cord that were coupled by net reciprocal inhibition. With relatively weak reciprocal coupling, a brief unilateral descending excitatory input to one oscillator produced effects ipsilaterally, but there was little effect on the contralateral oscillator. Turninglike patterns could be produced by each of the following modifications of the model: 1) unilateral descending input and relatively strong reciprocal coupling; 2) unilateral descending input that phase shifted as well as increased the amplitude of the waveform generated by an oscillator on one side; and 3) brief descending modulatory inputs that excited the oscillator on one side and inhibited the contralateral oscillator. In all three cases, there was an increase in "burst" duration ipsilateral to the excitatory input and an increase in cycle time, similar to turning locomotor activity in whole animals. It is likely that turning maneuvers are mediated by descending modulatory inputs primarily to the spinal oscillator networks, which control the timing of burst activity, but perhaps also to motoneurons for axial musculature.
The motor pattern for locomotion is produced by spinal locomotor networks that are thought to include three main components: central pattern generators consisting of unit oscillators that are distributed along the spinal cord and that generate the basic motor pattern; a spinal coordinating system that couples the oscillators to ensure proper timing of locomotor activity in different regions of the cord; and motoneurons that activate muscle and produce movement (reviewed in Grillner 1981 Muscle recordings in whole animals
Larval sea lamprey (Petromyzon marinus, 105-136 mm, n = 8 animals) were anesthetized in tricaine methanesulphonate (
In vitro brain/spinal cord preparations
Turning motor activity was investigated with in vitro brain/spinal cord preparations to eliminate contributions from mechanosensory inputs. Larval sea lamprey (100-142 mm, n = 18 animals) were anesthetized in tricaine methanesulphonate (MS222, 100-200 mg/l). The body below the anus was discarded, and most of the body musculature surrounding the notochord was removed. The brain and spinal cord, which were supported by the ventral cranium and notochord, respectively, were exposed. The preparation was transferred dorsal side up to a recording chamber containing oxygenated lamprey Ringer solution maintained at 6-9°C (McClellan 1990
CHEMICAL MICROSTIMULATION.
In vitro spinal locomotor activity was initiated by chemical microstimulation in brain locomotor regions as previously described (Hagevik and McClellan 1994
ELECTRICAL STIMULATION OF THE ORAL HOOD.
In intact lampreys, stimulation of one side of the oral hood (i.e., rostral part of head) produces turning to the opposite side, away from the stimulus, followed by escape swimming (McClellan 1984 UNILATERAL STIMULATION IN BRAIN STEM LOCOMOTOR REGIONS.
In several "lower" vertebrates (dogfish, fish, stingray, and sometimes turtle), continuous unilateral stimulation in brain locomotor regions elicits continuous asymmetric locomotor activity (Grillner and Wallén 1984 Analysis of turning motor activity
The main purpose of the present study was to examine the mechanisms responsible for the right-left asymmetries in locomotor activity during turning maneuvers in larval lamprey. However, changes in rostrocaudal phase lag during turning were also examined.
Data display and statistics
In whole animals, the values for a given locomotor parameter during turning for all animals were combined and plotted against turn angle to form scatter plots (Figs. 4, and 5; 66 turns, n = 8 animals). These data were analyzed with the use of Spearman Rank Correlations to determine whether there was a relationship between a given parameter and turn angle.
Computer modeling
BASIC MODEL CONFIGURATION.
Experimental results suggest that the central pattern generators in the lamprey spinal cord consist of right and left unit oscillators that are connected by net reciprocal inhibition (Fig. 1A) (Cohen and Harris-Warrick 1984
BIASING THE RIGHT AND LEFT OSCILLATORS.
To investigate possible mechanisms for turning in the present model, descending modulatory synaptic inputs were applied to one or both oscillators (Fig. 1A). Initially, five mechanisms for descending modulation of the oscillators were tested that might produce turninglike patterns to the right: 1) brief unilateral descending synaptic input (excitatory) that only phase shifted the right oscillator; 2) brief unilateral excitatory input that phase shifted as well as increased the amplitude of the waveform generated by the right oscillator; 3) brief bilateral descending synaptic inputs that excited the right oscillator and inhibited the left oscillator; 4) continuous bilateral synaptic inputs that excited the right oscillator and inhibited the left oscillator; and 5) bilateral inputs that caused a positive shift (i.e., depolarization) in the waveform of the right oscillator and a negative shift (i.e., hyperpolarization) in the waveform of the left oscillator. Preliminary computer simulations indicated that 4 and 5 did not produce changes in the oscillator waveforms that were similar to the motor patterns during turning behavior in whole animals (see Figs. 2 and 3). Therefore the first three mechanisms were investigated in more detail.
Turning maneuvers in whole animals
In larval lamprey, straight swimming is characterized by two features (Fig. 2, A and B): right-left bending of the body and undulations that travel from the head to the tail with increasing amplitude (Fig. 2B, 1st 4 frames) (McClellan 1990 RELATIVELY SMALL TURN ANGLES.
During swimming, spontaneous turns with small-to-moderate angles (<90°) began with slightly larger-than-normal bending of the head toward the side ipsilateral to the turn (Fig. 2, A and B, starting with frame 7, marked by arrow). The slightly larger-than-normal lateral deflection of the rostral body (frame 8) subsequently propagated to the middle (frame 9) and caudal body (frame 10) as the undulations traveled toward the tail. During turning, progressively more caudal areas of the body became aligned with the new axis of swimming, and the turns usually were completed within one cycle (frames 7-12). Animals very rarely produced continuous turning movements along an arc during several locomotor cycles. During the turn cycle (Fig. 2C1, *), rostral muscle burst activity on the side ipsilateral to the turn (2 in Fig. 2, C1 and C2) was larger in amplitude and longer in duration compared with control bursts recorded from the same sites during straight control swimming (Fig. 4A, same-side ratio) or compared with bursts in contralateral musculature during the turn cycle (Fig. 4B, right-left ratio). There was little change in contralateral muscle activity during the turn cycle (1 and 4 in Fig. 2C1). Locomotor bursts with longer durations and larger amplitudes on one side of the body should produce asymmetries in muscle contraction force that would be expected to turn the body to that side.
RELATIVELY LARGE TURN ANGLES.
During swimming, spontaneous turns with relatively large angles (>90°) were, for the most part, similar to those described above, but the asymmetries in movement and muscle activity were greater (Fig. 3, A and B, starting with frame 7, marked by arrow). In addition, there was often a brief pause before initiation of a turn with a large angle. In the example shown, the initial bending of the body was so great that the tip of the head almost touched the lower body (Fig. 3B, frames 7-9). The much larger-than-normal lateral deflection of the rostral body (frame 8) subsequently propagated to the middle body (frames 9/10) and then to the caudal body (frame 11) as the undulations traveled toward the tail. The turn was complete and the body was aligned with the new axis of swimming within one cycle (frames 7-12). During the turn cycle (Fig. 3C1, *), muscle burst activity on the side ipsilateral to the turn (2 and 3 in Fig. 3, C1 and C2) was larger in amplitude and longer in duration compared with control cycles preceding the turn (Fig. 4A) or compared with bursts in contralateral muscles during the turn cycle (Fig. 4B). After a turn with a large angle, the amplitude of muscle burst activity on the side contralateral to the turn often was increased relative to bursts in preceding and subsequent cycles (burst in 1 following * in Fig. 3C1). After an initial large deflection of the head to one side at the start of a turn, augmented contralateral bursts would be expected to decelerate the head to begin bending movements to the opposite side (Fig. 3B, frames 10/11).
PARAMETERS OF LOCOMOTOR ACTIVITY VERSUS TURN ANGLE.
In whole animals, the normalized parameters of locomotor activity during turning movements were pooled and plotted against turn angle (Figs. 4 and 5). During turning to one side, the same-side ratios for burst duration and burst amplitude increased significantly (P < 0.05 and P < 0.002, respectively; Spearman rank correlations, see METHODS) with increasing turn angle (Fig. 4A), as shown in Figs. 2 and 3.
Asymmetric locomotor activity in in vitro preparations
BRIEF ELECTRICAL STIMULATION OF THE ORAL HOOD.
Symmetrical chemical microstimulation was applied to right and left brain stem locomotor regions (see Fig. 6A) to produce symmetrical in vitro locomotor activity (see METHODS). Brief electrical stimulation (STIM) was applied to the left side of the oral hood at the onset of burst activity in a right rostral ventral root (2 in Fig. 6A; n = 9; see METHODS). Under these conditions, stimulation produced an increase in the same-side ratios for burst duration and burst amplitude during the perturbed cycle (2 in Fig. 6, B-D; Fig. 7, A and C; Table 1). This increase in burst duration resulted in a delay in the left burst (1) and an increase in the cycle time of the perturbed cycle (Fig. 7B, Table 1). The cycle times following the perturbed cycle often were similar to the control values preceding the perturbation. In some cases, the rhythm following the perturbed cycle consisted of slightly larger bursts with shorter cycle times than prestimulus activity. This faster, larger amplitude rhythm may represent escape swimming in response to stimulation of the oral hood (McClellan 1984 ASYMMETRIC CHEMICAL MICROSTIMULATION IN BRAIN STEM LOCOMOTOR REGIONS.
Continuous unilateral microstimulation in brain locomotor regions elicits asymmetric burst activity in several lower vertebrates, including dogfish (Grillner and Wallén 1984 Computer modeling
In in vitro preparations, brief stimulation of the oral hood resulted in changes in locomotor activity (Fig. 6) that were similar to turning motor activity in whole animals (Figs. 2 and 3). Although descending inputs to motoneurons might contribute to turning behavior (Fig. 1A), it is more likely that inputs to the oscillator networks are the main mechanism for initiating turning motor activity (see DISCUSSION). Therefore computer simulations were used to determine whether brief "descending" modulatory inputs from the brain to the oscillators could produce turninglike patterns.
UNILATERAL DESCENDING MODULATORY INPUT AND WEAK RECIPROCAL COUPLING.
With relatively weak reciprocal coupling between left and right oscillators (net reciprocal inhibition = 0.45), unilateral descending modulatory inputs that only phase shifted one oscillator did not produce turninglike patterns. Specifically, a descending excitatory input applied only to the right oscillator (Fig. 9A) during its positive phase (i.e., burst) resulted in an increase in the burst duration of the right oscillator (Fig. 9B). The burst duration increased with an increase in the amplitude of the descending input (Fig. 9C). However, the negative phase (i.e., silent period) of the left oscillator was only slighty affected, and this resulted in an increase in the right-left phase value and very little change in cycle time (Fig. 9D).
UNILATERAL DESCENDING INPUT AND STRONG RECIPROCAL COUPLING.
If the coupling between left and right oscillators was relatively strong (net reciprocal inhibition = 0.90) compared with Fig. 9, turninglike patterns could be produced in response to unilateral descending inputs that only phase shifted one oscillator (Fig. 10, A and B). In particular, a descending excitatory input applied only to the right oscillator during its positive phase (i.e., burst) resulted in an increase in the duration of the burst of the right oscillator as well as the negative phase (i.e., silent period) of the left oscillator (Fig. 10B). During the perturbed cycle, the normalized burst duration of the right oscillator and the overall cycle time increased with increases in the amplitude of the descending synaptic input (Fig. 10, C and D). In addition, with relatively strong reciprocal coupling, the burst duration and cycle time during the perturbed cycle could be controlled by the duration of the descending input pulse (D = 0.5 s and D = 1.0 s; Fig. 10, C and D).
UNILATERAL DESCENDING INPUT THAT INCREASE WAVEFORM AMPLITUDE.
With relatively weak reciprocal coupling (net reciprocal inhibition = 0.45), turninglike patterns could be produced if a unilateral descending excitatory input phase shifted as well as increased the amplitude of the waveform of the right oscillator (Fig. 11, A and B). The increased amplitude of the waveform generated by the right oscillator provided additional crossed inhibition that resulted in an increase in the duration of the silent period generated by the left oscillator (Fig. 11B). The burst duration of the right oscillator and the cycle time increased with increases in the amplitude as well as the duration (D = 0.5, D = 1.0) of the unilateral descending input pulse (Fig. 11, C and D).
BILATERAL MODULATORY INPUTS TO THE OSCILLATORS.
With relatively weak reciprocal coupling (net reciprocal inhibition = 0.45), turninglike patterns also could be produced if a relatively brief descending excitatory synaptic input was applied to the right oscillator during its positive phase (i.e., burst) and a brief descending inhibitory input was applied to the left oscillator during its negative phase (i.e., silent period). It is likely that descending brain neurons can directly excite neurons in the spinal locomotor networks ipsilateral to the turn (Buchanan et al. 1987 Summary of turning behavior in larval lamprey
During ongoing swimming, spontaneous turning behavior is initiated by a larger-than-normal deflection of the head to one side, similar to the photic turning response seen in adult lamprey (Ullen et al. 1993
Mechanisms for turning behavior in whole animals
DESCENDING INPUTS TO LOCOMOTOR OSCILLATOR NETWORKS.
During turning there are changes in both intensity (i.e., amplitude) and timing (i.e., burst duration, cycle time, right-left phase) of locomotor activity. In theory, all of these changes in locomotor activity can be produced by descending modulatory inputs to locomotor oscillator networks in the spinal cord. First, descending modulatory inputs could increase the activity of interneurons in the spinal locomotor oscillators on the side ipsilateral to the turn that would then be expected to increase the intensity of locomotor burst activity in motoneurons on the same side. Second, descending modulatory inputs to the spinal locomotor oscillators are the most direct mechanism for producing the changes in timing of locomotor activity associated with turning. For example, in the computer model, brief descending inputs of opposite polarity applied to the right and left oscillators resulted in an increase in the cycle time and burst duration during the perturbed cycle (Fig. 12, C and D), similar to those seen during turning locomotor activity in whole animals (Figs. 2-5). In whole animals there was an increase in right-left phase value during turning (Fig. 5), an effect that was not seen in the computer simulations. However, at least part of the increase in right-left phase value appeared to be due to an increase in the burst delay (Fig. 5C) that resulted in a pause before initiation of the turn. With the present computer model, it was not possible to simulate these discontinuities in the motor pattern.
DESCENDING INPUTS TO SPINAL MOTONEURONS.
Descending inputs to motoneurons certainly can produce changes in the intensity of locomotor output. However, it is unlikely that descending modulation of motoneurons is the primary mechanism for the changes in timing of locomotor activity during turning, because motoneurons probably are not part of the oscillator mechanism in lamprey (Wallén and Lansner 1984 Asymmetric in vitro locomotor activity
SENSORY-EVOKED TURNINGLIKE ACTIVITY.
In in vitro preparations, brief stimulation of one side of the oral hood produced changes in ongoing locomotor activity, such as an increase in burst duration, burst amplitude, and cycle time (Figs. 6 and 7; Table 1), similar to those during spontaneous turning in whole animals (Figs. 2-4). Because sensory-evoked turning activity in in vitro preparations had several features in common with spontaneous turning in whole animals, this in vitro paradigm will be useful for examining the brain stem and spinal systems involved in mediating turninglike motor activity.
Other aspects of turning maneuevers
TURNING MOTOR ACTIVITY ALONG THE BODY.
Although our analysis of turning focused on changes in motor activity recorded from the rostral body, similar changes often occurred in burst activity from more caudal recording sites (e.g., Fig. 3). One possibility is that the descending systems that produce turning directly affect the locomotor networks along the entire spinal cord. A second possibility is that descending systems for turning directly affect the rostral spinal locomotor networks, and asymmetries in locomotor activity in this part of the spinal cord are then transmitted to more caudal networks through descending spinal pathways.
DESCENDING NEURONS THAT MEDIATE TURNING BEHAVIOR.
In the present study, it was not possible to use partial lesions of the spinal cord to determine which descending pathways mediate turning because of the likely possibility of also interrupting descending initiation pathways. Therefore at present it is not known which descending pathways mediate turning and whether these pathways are similar or distinct from descending initiation pathways for locomotion (McClellan 1988 Comparisons with other studies
LAMPREY.
In adult lamprey that are either quiescent or actively swimming, light originating from one side elicits a negative phototaxic response in which an animal turns away from the stimulus (Ullen et al. 1993 OTHER VERTEBRATES.
Gray (1933) INVERTEBRATES.
In the locust, descending brain interneurons (DNI, DNM, and DNC) respond to visual, ocellar, wind, and mechanosensory inputs and make connections with premotor interneurons in the flight system and thoracic motoneurons to execute steering maneuvers (Reichert and Rowell 1985 Conclusions
During swimming in larval lamprey, spontaneous turning maneuvers were produced by larger-than-normal bending of the head to one side, followed by undulations that propagated down the body with greater amplitude on the side ipsilateral to the turn. During turning to one side, the burst amplitudes and burst durations of muscle activity ipsilateral to the turn as well as cycle times increased significantly with increasing turn angle. In in vitro brain/spinal cord preparations, brief electrical stimulation applied to the side of the oral hood produced several changes in the locomotor pattern that were similar to those seen during turning in whole animals. In contrast, unilateral brain stem stimulation elicited asymmetric motor activity but, at least for the sites used in the present study, did not produce significant changes in cycle time, as occurs during the single cycles of turning activity in whole animals. Computer model simulations, in which brief excitatory descending inputs were applied to one oscillator and the contralateral oscillator received inhibition, produced changes in the rhythmic output patterns that were similar to those observed during turning motor activity in whole animals.
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Stein 1978). Brain stem command or initiation systems activate the spinal locomotor networks and initiate locomotor behavior (reviewed in Grillner 1981; McClellan 1986; Stein 1978). In addition, descending systems modulate spinal locomotor networks to produce a number of adaptive variations in locomotor behavior, such as acceleration, deceleration, turning, steering (i.e., small course adjustments), and equilibrium control.
). During straight swimming, the side-to-side bending of the body is approximately symmetrical. Turning maneuvers are produced by an initial larger-than-normal bending of the head to one side (Gray 1933). Subsequently, undulations pass down the body with greater amplitude on the side ipsilateral to the turn.
; Grillner and Kashin 1976; also see Wallén et al. 1985). However, descending modulatory inputs to motoneurons, which are not thought to be part of the oscillator networks (see Wallén and Lansner 1984), would be expected primarily to affect the intensity (i.e., amplitude) of locomotor bursts with perhaps little or no direct effect on the cycle time of the locomotor activity (however, see DISCUSSION). In contrast, descending modulatory inputs to the oscillators could affect intensity (i.e., burst amplitude) as well as timing (i.e., burst duration, cycle time) of locomotor activity. Descending inputs to both motoneurons and interneurons are thought to produce steering maneuvers in flying insects (Burrows and Pfluger 1992; Gronenberg and Strausfeld 1990; Reichert and Rowell 1985; Rowell and Reichert 1986).
).
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
100-200 mg/l), and pairs of fine copper wires (56 µm diam) insulated except at the tip were implanted beneath the skin in rostral (electrodes 1 and 2) and middle (electrodes 3 and 4) body musculature (see Fig. 2A) as previously described (Davis et al. 1993). Locomotor movements of freely swimming animals were videotaped with an S-VHS camera (Panasonic PVS770 camcorder) mounted 125 cm above the recording chamber and were stored on S-VHS tape (JVC HR 6700U recorder). Simultaneously, muscle activity was recorded, amplified, and stored on VHS tape (Neuro-Data DR886). A special electronic instrument detected each video frame and generated a sync pulse that incremented a light-emitting diode counter that was visible in the video field. These sync pulses also were used to create a pulse code that identified the frame number and that was recorded on one of the channels with muscle activity. In this way it was possible to index each video frame with a point in time on the record for muscle activity (see Figs. 2 and 3). After the recordings, the number of body segments between the rostral and caudal electrodes was counted.
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FIG. 2.
Locomotor movements and activity in whole animal during 45° turn to right. A: diagram of animal (length = 107 mm) showing positions of muscle recording electrodes at 28% body length (BL; 1-2) and 50% BL (3-4). B: sequential video frames (interframe interval = 67 ms) during turning to right, starting at frame marked by arrow. Dots: lateral shift of each frame; frames correspond in time to dots in C1. C: muscle activity before, during (*), and after turn cycle, as shown in B. C1: "raw" muscle activity. C2: same activity integrated ( 
= 10 ms). Locomotor pattern consisted of right-left alternation (1-2 and 3-4) and rostrocaudal phase lag (1-4 and 2-3). During turn cycle (*), amplitude and duration of burst activity ipsilateral to turn (2) increased compared with cycles before or after turn, and there was an increase in cycle time.
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FIG. 3.
Locomotor activity in whole animal during 135° turn to right (see legend for Fig. 2). A: diagram of animal (length = 115 mm) showing positions of muscle recording electrodes at 23% BL (1-2) and 48% BL(3-4). B: sequential video frames (interframe interval = 133 ms) during turning to right starting at frame marked by arrow. C: muscle activity before, during (*), and after turn cycle, as shown in B. C1: raw muscle activity. C2: integrated activity ( = 10 ms). During turn cycle (*), amplitudes and durations of burst activity ipsilateral to turn (2 and 3) increased compared with cycles before or after turn, and there was an increase in cycle time. In addition, immediately after turn, amplitude of burst contralateral to turn (1) was larger than normal.
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FIG. 4.
Comparison of locomotor parameters in whole animals during turns of various angles (see METHODS). A: normalized same-side ratios for (A1) burst duration and (A2) burst amplitude (n = 66 turns, 8 animals) increased significantly with increasing turn angle (P < 0.05 and P < 0.002, respectively; Spearman rank correlations, see RESULTS). B: normalized right-left ratios for (B1) burst duration and (B2) burst amplitude increased significantly (P < 0.05 and P < 0.002, respectively) with increasing turn angle (Spearman rank correlations).
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FIG. 5.
Right-left phase values during turns of various angles in whole animals. During turn cycles, (A) right-left phase values (burst delay divided by cycle time), (B) normalized cycle times, and (C) normalized burst delay (delay from left burst to right burst) increased significantly (P < 0.05, P < 0.05, and P < 0.002, respectively) with increasing turn angle (Spearman rank correlations, see RESULTS).
). The choroid plexus was removed over the third and fourth ventricles, and the cerebellar commissure was cut to expose the brain for chemical microstimulation (see below). The Ringer solution contained d-tubocurarine (15 mg/l) to block possible contractions in the remaining musculature around the cranium and notochord. Suction electrodes (e.g., 1-4 in Fig. 6A) were placed in contact with ventral roots to record locomotor activity, which was amplified and stored on VHS tape (NeurodataDR-890).
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FIG. 6.
Effects of sensory stimulation of oral hood during in vitro locomotor activity. A: in vitro brain/spinal cord preparation showing ventral root electrodes at segment 11 (1-2) and segment 41 (3-4) from larval lamprey (animal length = 110 mm). Left (SL) and right (SR) micropipettes were positioned in left and right brain locomotor regions, and locomotor activity was elicited by symmetrical chemical microstimulation. Brief electrical stimulation (STIM) was applied to left side of oral hood at onset of burst activity in electrode 2. B-D: during brain stimulation (S), brief oral hood stimulation ( 
) resulted in an increase in duration of right burst (2) and an increase in cycle time. Dots above each record: timing of average cycle time before perturbed cycle. There was also an increase in amplitude of right burst (2). Normalized burst duration/cycle time increased by 45%/25% (50 µA), 120%/51% (100 µA), and 147%/74% (200 µA) for increasing stimulation current (see Fig. 7).
; McClellan 1986, 1994). This technique is thought to directly or indirectly excite neurons in the brain locomotor command system that then activate spinal locomotor networks and initiate locomotor activity (Hagevik et al. 1996). The stimulating micropipettes contained either 5 mM D-glutamate or a 5 mM D-glutamate/5 mM D-aspartate mixture in Ringer solution (pH adjusted to 7.2-7.4), with Fast Green added to visualize the agents when ejected into the brain stem. The micropipettes were broken off to a tip diameter of 1-5 µm, and the tips were positioned ~25-50 µm below the dorsal surface of the brain, usually in the rostrolateral rhombencephalon (see Hagevik and McClellan 1994; McClellan 1994). Two micropipettes were symmetrically positioned for bilateral stimulation in right and left brain stem areas (see Figs. 6A and 8A). The amount of excitatory agent that was ejected from each micropipette was visually adjusted by varying the durations of pressure pulses (10- to 30-ms pulses delivered at 1 Hz; 10-20 psi, same pressure applied to each micropipette) to control the size of the ejection bolus within the tissue. In general, each pressure pulse ejected a bolus with a diameter of 25-50 µm (0.008-0.065 nl), and the diameter of the ejection area stained with Fast Green at the end of stimulation was usually less than 100 µm (width of brain 1 mm). The recording chamber (volume 60 ml) was periodically flushed with fresh Ringer solution.
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FIG. 8.
In vitro locomotor activity during symmetrical and unilateral chemical microstimulation in brain locomotor regions. A: in vitro brain/spinal cord preparation showing ventral root electrodes at segment 10 (1-2) from larval lamprey (animal length = 129 mm). Left and right micropipettes for chemical microstimulation were positioned in left and right brain locomotor regions. B: symmetrical chemical microstimulation in right and left brain locomotor regions elicited approximately symmetrical alternating right-left locomotor activity (1 and 2). C and D: unilateral chemical microstimulation applied only to left (C) or right (D) side of brain produced locomotor bursts that were larger in amplitude and longer in duration on side ipsilateral to stimulation than those elicited by symmetrical stimulation in B. However, there was little change in cycle time, as occurs during turning in whole animals.
, 1990). Therefore brief electrical stimulation was applied to the left side of the oral hood during symmetrical brain-stem-initiated in vitro locomotor activity (n = 9 animals). Preliminary results indicated that stimulation of the left side of the oral hood at the onset of burst activity on the right side of the spinal cord produced the largest increases in cycle time and right burst duration, similar to turning motor activity in whole animals. In contrast, stimulation during other phases of the rhythm produced comparatively smaller changes in the timing of locomotor activity. In the in vitro experiments, a threshold detector was used to detect the onsets of locomotor bursts recorded in a right, rostral ventral root (2 in Fig. 6A). The threshold detector then triggered a stimulator that, in conjunction with a stimulus isolation unit, delivered a train of biphasic current pulses to the left side of the oral hood (5-500 µA; positive 2-ms and negative 2-ms current pulses separated by 1 ms and delivered every 10 ms for a total of 50 ms). The stimulation electrode consisted of two insulated copper wires (0.41 mm diam) whose tips were separated by 1.5 mm. Following stimulation there were 
6-10 locomotor cycles before another stimulus train was delivered. During playback, the locomotor activity was electronically blanked during the relatively short periods when stimulus pulses were delivered. Using biphasic current pulses and selectively blanking the locomotor activity reduced stimulus artifacts sufficiently so that the timing of locomotor bursts could be analyzed (see Fig. 6B, ). Because different in vitro preparations displayed different sensitivities to electrical stimulation of the oral hood, in each experiment the range of stimulus currents that produced observable changes in locomotor activity was determined empirically.
; Kashin et al. 1974; Kazennikov et al. 1979; Livingston and Leonard 1990) that may be related to turning maneuvers (see Grillner and Wallén 1984). Therefore, in the lamprey, unilateral chemical microstimulation was used to test whether asymmetric activation of brain locomotor regions could produce changes in motor activity that were similar to those that occur during the single cycles of turning activity in whole animals. Asymmetric chemical microstimulation (n = 9 animals) was produced by stimulating either in left or right brain locomotor regions (see Fig. 8A). In general, unilateral stimulation had to be maintained over many seconds before a stable asymmetric locomotor pattern was established (e.g., Fig. 8, C, right and D, right).
= 10 ms, whereas for in vitro activity = 50 ms was used (see below). Motor activity was played out with the use of a thermal array chart recorder (Gould TA2000) at 10 mm/s (in vitro activity) or 50 mm/s (muscle activity). The onsets, offsets, and peaks of locomotor bursts were marked on a digitizing pad with the use of interactive software, and data arrays were imported into a spreadsheet for performing calculations and creating graphs. For simplicity of analysis, it was desirable to have all turninglike motor activity correspond to "right turns." Therefore, in whole animals, the measurements for turns to the left were reversed to match those for right turns so that all turns could be described under a single category, right turns. Locomotor activity in in vitro preparations was modulated to mimic right turns.
= 10 ms time constant were calculated to be <6%. For in vitro activity, 60 ms was subtracted from the burst durations so that the errors in normalized burst durations were calculated to be <4%.
).
View this table:
TABLE 1.
Parameters of locomotor activity during brief electrical stimulation on the left side of the oral hood
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FIG. 7.
Average parameters for turning locomotor activity from in vitro preparation BA27 (same animal as in Fig. 6 and Table 1) vs. strength of brief electrical stimulation (STIM. CURRENT) applied to oral hood (50 µA, n = 7 perturbed cycles; 100 µA, n = 7; 200 µA, n = 5). Black bars: parameters during perturbed cycles. White bars: control cycles preceding stimulation. Normalized same-side ratio for burst duration (A; 2 in Fig. 6), normalized cycle times (B), and normalized same-side ratio for burst amplitude (C) increased with increases in stimulus current. D: right-left phase values were ~0.5 during perturbed cycle and during control cycles. At each current level, t-test was used to compare average locomotor parameters during perturbed cycle with those during preceding control cycles. Single asterisk: P < 0.05. Double asterisk: P < 0.01. Triple asterisk: P < 0.002. See text and Table 1 for statistical analysis of data from all preparations.
; Hagevik and McClellan 1994). The spinal locomotor networks are activated and modulated by descending inputs that probably bias the spinal oscillator networks and/or motoneurons to produce asymmetric motor activity and turning behavior (Fig. 1A). In the present study, descending modulatory inputs were applied to a right-left pair of coupled oscillators to determine whether these inputs could produce asymmetric waveform patterns similar to those seen during turning behavior in whole animals.
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FIG. 1.
Setup for computer model. A: left and right oscillators are connected by reciprocal inhibition ( 
) in parallel with weaker reciprocal excitation (short bars) (see Hagevik and McClellan 1994). In theory, descending modulatory inputs to spinal oscillator networks and/or motoneurons might elicit asymmetric motor activity and turning maneuvers. In present model only descending modulatory inputs to oscillators were examined, because these inputs would be expected to produce changes in both intensity and timing of locomotor activity that occur during turning behavior. It is not known whether descending modulatory systems for turning are separate or overlap with descending initiation pathways for locomotion (not shown). B: phase oscillator consisting of vector that rotates around origin with cycle time, T. Output of an oscillator at given point in time is proportional to sine of phase angle at that time. C: phase response curves (PRCs) for excitatory (PRCE) and inhibitory (PRCI) synaptic inputs to an oscillator (see text).
; McClellan and Jang 1993), which consisted of a vector that rotated around the origin with a cycle time, T. The phase angle, 
i+1, at a given point in time is given by
The term
(1)
i represents the previous phase value; the second term is the phase increment due to rotation of the vector during the time increment 
t. The third term is the phase shift due to synaptic inputs and determined from the phase response curves (PRCs). The output waveform of a particular oscillator is given by
where B is an amplitude scaling factor, usually set to 1.0.
(2)
). The experimental PRCs were normalized to an amplitude of 1.0, and the shapes of the PRCs were modified slightly so that they could be described by simple mathematical functions (Fig. 1C). There are at least three reasons that justify the use of these PRCs: First, although these PRCs are adopted from "simple" neuronal oscillators, which may be less complex than the locomotor networks in the lamprey spinal cord, the PRCs do result in oscillator output patterns that would be expected for certain types of synaptic connections (Hagevik and McClellan 1994; McClellan and Jang 1993). If the PRCs were drastically different from those used here, it is unlikely that the model would generate realistic output patterns. Second, in the proposed model for the locomotor central pattern generator in the lamprey spinal cord (Grillner et al. 1988), commissural interneurons (Buchanan 1982) are connected by reciprocal inhibition and are involved in controlling the timing of right-left alternation of locomotor activity. Thus descending inputs to commissural interneurons are the most direct mechanism for producing the changes in timing of locomotor activity that occur during turning. The commissural interneurons probably have PRCs similar to those used in the present study (Wallén and Grillner 1985, 1987). Third, to generate turning patterns, the PRCE should have a region of phase delay during the early, positive phase of the cycle (Fig. 1C) so that brief descending excitation applied to an oscillator on one side (right) during this time will increase "burst" duration (Fig. 12B). Likewise, the PRCI should have a region of phase delay during the late, negative phase of the cycle (Fig. 1C) so that inhibition applied to the contralateral (left) oscillator during this time will increase the "silent" period (see Fig. 12B).
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FIG. 12.
A: computer model showing right and left oscillators connected by relatively weak reciprocal coupling (net reciprocal inhibition = 0.45). Descending excitatory synaptic input was applied to right oscillator and inhibitory input (DL) was applied to left oscillator (see RESULTS). B: brief descending inputs of opposite polarity (DR = +2.0, DL = 
2.0; durations = 0.5 s) applied at start of positive phase of right oscillator. Positive phase (i.e., burst duration) of right oscillator and negative phase (i.e., silent period) of left oscillator increased in duration. C and D: during perturbed cycle, (C) normalized burst duration of right oscillator and (D) overall cycle time increased with increases in amplitude of descending synaptic input for both short (D = 0.5 s) and longer (D = 1.0 s) inputs.
). Each oscillator summed the excitatory and inhibitory synaptic inputs that occurred at a particular stimulus phase for that oscillator. If the net synaptic input was positive (i.e., depolarization), the phase of the oscillator was shifted by an amount derived from PRCE at the stimulus phase, whereas if the net synaptic input was negative (hyperpolarization), the phase shift was determined by PRCI (Fig. 1C), as previously described (Hagevik and McClellan 1994).
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
). At a given point along the body, the lateral movements to the right and left are approximately equal in amplitude (Davis et al. 1993). The above two features of locomotor movements are produced by two features of locomotor activity (Fig. 2, C and D, 1st 3 cycles): right-left alternation of motor activity at the same segmental level (1-2 and 3-4), and a rostrocaudal phase lag of burst activity on the same side of the body (1-4 and 2-3).
0.5 (Fig. 5A), as would be expected for symmetrical alternating locomotor activity. The right-left phase values increased significantly with increasing turn angle (Fig. 5A; P < 0.05; Spearman rank correlations). The apparent leveling off of right-left phase values at the largest turn angles may reflect the relatively few data points for these turns. In theory, an increase in right-left phase value could be due to changes in cycle time, burst delay, or both (see METHODS). Although both normalized cycle time and normalized burst delay increased significantly (P < 0.05 and P < 0.002, respectively) with increasing turn angle (Fig. 5, B and C), the burst delay increased to a larger degree and accounted for the increase in right-left phase value (Fig. 5A). Presumably, the increase in burst delay, particularly during large turn angles, is related to the pause that occurs before such turns (see above).
, 1990).
), fish (Kashin et al. 1974), stingray (Livingston and Leonard 1990), and sometimes turtle (Kazennikov et al. 1979). This asymmetric activity may be related to turning (Grillner and Wallén 1984). Therefore, in the lamprey, unilateral brain stem stimulation was used to test whether asymmetric activation of brain stem locomotor regions could produce the types of changes in motor activity that occur during the single cycles of turning activity in whole animals. First, symmetrical chemical microstimulation in right and left brain stem locomotor regions usually initiated relatively symmetrical in vitro locomotor activity (Fig. 8, A and B; see METHODS). Second, when chemical stimulation was applied to one side of the brain stem (n = 9), the burst durations and burst amplitudes on the same side increased relative to those during symmetrical stimulation (Fig. 8, C and D). In general, unilateral stimulation had to be maintained for many seconds before a stable asymmetric locomotor pattern was established (e.g., Fig. 8, C and D, right). However, unilateral brain stem stimulation, at least with the sites used in the present study, did not produce significant changes in cycle time, as occurs during the single cycles of turning activity in whole animals.
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FIG. 9.
A: computer model showing right and left oscillators connected by relatively weak reciprocal coupling (net reciprocal inhibition = 0.45; excitation = 0.60 in parallel with inhibition = 1.05). Brief unilateral descending modulatory input (DR) only phase shifted right oscillator. B: brief descending input (amplitude = 2.0; duration = 0.5 s) applied at start of positive phase ("burst") of right oscillator increased burst duration of this oscillator, but there was little effect on left oscillator. C and D: during perturbed cycle, normalized burst duration of right oscillator increased with increases in amplitude of descending synaptic input, but there was little change in cycle time.
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FIG. 10.
A: computer model showing right and left oscillators connected by relatively strong reciprocal coupling (net reciprocal inhibition = 0.90; excitation = 1.20 in parallel with inhibition = 2.10). Brief unilateral descending modulatory input only phase shifted right oscillator. B: brief descending input (amplitude = 2.0; duration = 0.5 s) applied at start of positive phase (burst) of right oscillator increased burst duration of this oscillator, and increased "silent" period of the left oscillator. C and D: during perturbed cycle, (C) normalized burst duration of right oscillator and (D) overall cycle time increased with increases in amplitude of descending synaptic input. In addition, burst duration and cycle time could be controlled by duration of descending input pulse (D = 0.5 s, D = 1.0 s).
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FIG. 11.
A: computer model showing right and left oscillators connected by relatively weak reciprocal coupling (net reciprocal inhibition = 0.45). Brief unilateral descending modulatory input phase shifted as well as increased amplitude of waveform generated by right oscillator. B: brief descending input (amplitude = 2.0; duration = 0.5 s) applied at start of positive phase (burst) of right oscillator increased burst duration of this oscillator as well as negative phase (i.e., silent period) of left oscillator. C and D: during perturbed cycle, (C) normalized burst duration of right oscillator and (D) overall cycle time increased with increases in amplitude of descending synaptic input for both short (D = 0.5 s) and longer (D = 1.0 s) inputs.
; Ohta and Grillner 1989; Rovainen 1979a). Descending inhibition of the contralateral spinal locomotor networks might result in at least three ways: 1) unilateral descending pathways that directly excite motor networks ipsilateral to the turn and indirectly inhibit the contralateral networks through crossed inhibitory spinal interneurons (Fig. 12A); 2) descending pathways contralateral to the turn that activate inhibitory descending propriospinal relay neurons; and 3) descending pathways contralateral to the turn that directly inhibit (Wannier et al. 1995) the motor networks on that side.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
). Subsequently, undulations propagate down the body with greater amplitude on the side ipsilateral to the turn. Thus, as the turn proceeds, progressively more caudal levels of the body align with the new axis of swimming (Figs. 2 and 3). Similar results have been seen during turning behavior in other fish (Gray 1933).
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FIG. 13.
Model of possible mechanisms by which descending modulatory inputs could produce asymmetric locomotor activity and turning maneuvers. Right and left oscillators are coupled by dominant reciprocal inhibition (see METHODS and legend to Fig. 1). Descending modulatory synaptic inputs to oscillators can produce changes in timing (i.e., burst duration, cycle time, right-left phase value) of locomotor activity, whereas direct and indirect inputs to motoneurons (MN) can produce changes in intensity (i.e., burst amplitude) of activity. It is not known whether descending modulatory systems for turning are separate or overlap with descending initiation pathways for locomotion (not shown). Descending modulatory inputs to motoneurons primarily would affect intensity of burst activity, but indirectly could affect timing because of changes in forces generated in muscle (see DISCUSSION). Because activation of mechanoreceptors during bending of body can shorten (i.e., phase advance) cycle time (McClellan and Jang 1993 ), during turning it may be necessary to gate effects of these sensory neurons on spinal locomotor networks to increase cycle time.
, 1982, 1984; McClellan and Jang 1993; McClellan and Sigvardt 1988). Resetting experiments indicate that under these conditions, activation of mechanoreceptors on the left side of the spinal cord will shorten the cycle time (i.e., phase advance) by exciting the left oscillators and inhibiting the right oscillators (McClellan and Jang 1993; McClellan and Sigvardt 1988). Thus an increase in burst intensity on the right side of the body should cause rapid bending of the body to that side, which would then prematurely terminate the right burst and prevent an increase in burst duration and cycle time, which are features of turning (Figs. 4 and 5). Therefore, to counter this effect during turning maneuvers, it may be necessary to reduce the sensitivity of the oscillators to mechanosensory input and/or gate the connections between mechanosensory neurons and the oscillators.
). During locomotor activity, the membrane potentials of motoneurons alternate between depolarization and hyperpolarization (Buchanan and Cohen 1982; Russell and Wallén 1983). Descending excitatory inputs to motoneurons during their depolarizing phase would be expected to increase directly the intensity (amplitude) of burst activity. However, this could also be accomplished indirectly by descending inputs to the oscillators (see above). Direct descending excitatory inputs to motoneurons during their depolarizing phase also could increase the duration of burst activity, but this increase would be limited without an accompanying mechanism to increase cycle time. For example, during large turn angles the burst durations recorded on the side ipsilateral to the turn can increase by much more than a factor of 2 (Fig. 4A1). However, descending inputs to motoneurons alone might produce small changes in the right-left symmetry of locomotor activity for equilibrium or minor steering adjustments (Wallén et al. 1985; also see Orlovsky et al. 1992; Rovainen 1979b), provided that there is little or no need for changes in the cycle time of locomotor activity.
).
), are involved in rapid biasing of the spinal motor networks to initiate turning maneuvers (Brodin et al. 1988). Stimulation of some Müller cells can slow down the locomotor rhythm (Vinay and Grillner 1993), whereas other neurons appear to speed up the rhythm (Buchanan and Cohen 1982). Although Müller cells might participate during swimming and turning maneuvers, they do not appear to be necessary for either maneuver (McClellan 1988).
; Wallén et al. 1994). During ongoing locomotion the turns are characterized by a larger-than-normal, laterally directed mechanical wave that passes down the body at a lower velocity than normal. In addition, there is an increase in the intensity and duration of muscle burst activity for turns >60° and a slowing down of the rhythm. These effects are similar to those seen in the present study during spontaneous turns in larval lamprey. Similar turning motor activity can occur under a variety of conditions, for example spontaneously (Figs. 2 and 3) as well as in response to tactile (Fig. 6) or photic stimuli (Ullen et al. 1993). Therefore it is likely that the same descending system(s) are involved in producing turning regardless of the stimulus.
examined turning behavior in a number of fish (eel, butterfish, dogfish, rudd, whiting, and goldfish) and found that this maneuver is produced by a larger-than-normal undulatory wave that propagates at a reduced rate down the body on the side ipsilateral to the turn. Thus, as the turn proceeds, progressively more caudal areas of the body become aligned with the new axis of swimming. In fish with relatively short, stiff bodies, the caudal fin is particularly important in stabilizing the position of the caudal half of the body so that the head and anterior half of the body can pivot. During slow turns, the pectoral fins appear to contribute but are not considered to be the main mechanism for changes in direction (however, see Harris 1936).
; Reichert et al. 1985; Rowell 1989; Rowell and Reichert 1986). In addition, sensory neurons that innervate head hairs activate wind-sensitive interneurons (A4I1) in the abdominal ganglia that make connections with flight motoneurons to steering muscles (Burrows and Pfluger 1992).
; Nolen and Hoy 1984). These effects are much weaker in nonflying insects and thus are dependent on behavioral context. Similar behavioral-context-dependent effects were seen for synaptic inputs to uropod motoneurons during steering, but only when these structures were engaged in postural movements (Takahata and Murayama 1992).
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ACKNOWLEDGEMENTS |
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We thank Dr. Richard Madsen, with assistance from Y. Li, for advice on statistics and for performing much of the statistical analysis; J. Scher, V. Gupta, T. Phan, and K. Paggett for help with data analysis; and D. Allen for providing comments on an earlier version of the manuscript. We are grateful to the Lamprey Control Units of the U.S. Fish and Wildlife Service at Millersburg, MI and Ludington, MI for helping with lamprey collection.
This work was supported by National Institute of Neurological Disorders and Stroke Grant NS-29043 and American Paralysis Association Grant MB1-9108 awarded to A. D. McClellan.
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FOOTNOTES |
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Address for reprint requests: A. D. McClellan, Division of Biological Science, 105 Lefevre Hall, University of Missouri, Columbia, MO 65211.
Received 16 August 1996; accepted in final form 31 March 1997.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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parallels to initiation of locomotion in mammals.
In: Wenner-Gren Symposium Series: Neurobiology of Vertebrate Locomotion,
edited by
S. Grillner,
R. Herman,
P. Stein,
and D. Stuart
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