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The Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institute, Stockholm, Sweden
Submitted 28 August 2006; accepted in final form 30 October 2006
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ABSTRACT |
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INTRODUCTION |
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). Postural corrections can be caused by changes of the body orientation in relation to gravity, as well as by body accelerations in the corresponding planes. These two types of stimuli are sensed by vestibular organs (Deliagina et al. 1992b; Lowenstein 1970). A detailed analysis of the roll and pitch control systems was done previously (Deliagina 1997a,b; Deliagina and Fagerstedt 2000; Deliagina et al. 1992a,b, 1993, 2000; Pavlova and Deliagina 2002; Zelenin et al. 2000, 2005). It was found that stabilization of the body orientation in each of the planes (roll and pitch) is based on the interaction of two antagonistic postural reflexes and the animal stabilizes the orientation at which the reflexes are equal to each other. In reality, orientation of the animal can be disturbed simultaneously in both planes. Interaction of the two control systems has not been analyzed, however.
In contrast to changes of body orientation in the vertical (roll and pitch) planes, turns in the yaw plane do not affect the animal's orientation in the gravity field and therefore gravity cannot be used as a reference direction. Do the vestibular reflexes driven by yaw-sensitive vestibular afferents (Lowenstein 1970; Lowenstein et al. 1968) yet play a role in the control of orientation in the yaw plane? In particular, what is their role when the animal's orientation in this plane is changed passively, e.g., under the effect of a water stream or when colliding with obstacles? Also, how do these reflexes interact with active changes of yaw orientation that occur during swimming arising from the periodical locomotor undulations of the head and body (Williams et al. 1989) or during lateral turns when the animal changes the direction of swimming by itself (Ullén et al. 1993, 1995b)? Investigation of the activity of vestibular-driven mechanisms controlling orientation of the lamprey in the yaw plane was the general goal of the present study.
In the lamprey, motor commands are transmitted from the brain to the spinal cord mainly by the reticulospinal (RS) pathways (Brodin et al. 1988; Bussiéres 1994; Nieuwenhuys 1972). The RS neurons receive vestibular input through interneurons of vestibular nuclei (Koyama et al. 1989; Northcutt 1979; Rovainen 1979). They also receive input from other sensory systems, from the forebrain, from different centers in the brain stem, and from the spinal cord (Deliagina et al. 1993; Dubuc et al. 1993; Rovainen 1967, 1979; Viana Di Prisco et al. 1995; Wickelgren 1977). The majority of axons of RS neurons project ipsilaterally and can reach even the most caudal segments of the spinal cord (Bussiéres 1994). They affect segmental interneurons and motoneurons (Buchanan and Cohen 1982; Ohta and Grillner 1989; Rovainen 1974; Wannier et al. 1998). Individual RS neurons exert diverse effects on spinal motor output (Zelenin et al. 2001, 2003). In a recent study by Zelenin et al. (2005), it was shown that individual RS neurons, activated by rotation in a definite plane, elicit the torque counteracting rotation that activated the neuron.
In the study by Zelenin et al. (2005), the population of RS neurons responding to yaw turn was revealed. Most of them were activated by the contralateral turn. However, in that study the vestibular responses of yaw-related RS neurons were not characterized in any detail. Also, the data were obtained on the in vitro preparation (consisting of the brain stem with labyrinths and rostral part of the spinal cord), in which a number of inputs to RS neurons, like those from the forebrain, from the cranial nerves, and from the caudal parts of the spinal cord, were abolished. The first aim of the present study was to examine in intact animals the activity of RS neurons related to the yaw control. For this purpose, we used the method of recording activity of RS neurons from their axons in the spinal cord by means of chronically implanted electrodes (Deliagina and Fagerstedt 2000; Deliagina et al. 2000). Responses of individual neurons were extracted from the multielectrode recording of the mass activity, using a spike-sorting procedure (Zelenin 2005).
It was shown earlier that RS neurons of the roll- and pitch-related populations receive their main vestibular input from the contralateral labyrinth (Deliagina and Pavlova 2002; Pavlova and Deliagina 2003). The second aim of the present study was to examine the relative role of the two labyrinths for generation of the yaw-related responses in RS neurons. For this purpose, we compared the RS responses to yaw turn in individual animals before and after a unilateral labyrinthectomy (UL).
It is known that unilateral eye illumination in the lamprey elicits a contralateral turn in the yaw plane (negative phototaxis) (Ullén et al. 1993, 1995b, 1997). The third aim of the present study was to reveal the RS neurons presumably involved in initiation of this response. For this purpose, we studied responses of RS neurons to unilateral eye illumination, as well as interactions of vestibular and visual inputs to these neurons. A brief account of this study was previously published in abstract form (Karayannidou et al. 2005).
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METHODS |
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Electrodes
The activity of RS neurons was recorded from their axons in the spinal cord by means of chronically implanted macroelectrodes similar to those described in previous papers (Deliagina and Fagerstedt 2000; Deliagina et al. 2000). The electrodes (silver wires, 75 µm in diameter and 2 mm in length) were oriented in parallel to the long spinal axons, thus allowing us to record the spike activity from fibers with a conduction velocity of >1.5 m/s.
The electrodes were glued onto a plastic plate [7.5 x 2.5 x 0.25 mm (length x width x thickness)]. For measuring the axon position and conduction velocity (see following text) we used a plate with four electrodes (Fig. 1 A). The distance between the left and right electrodes was 1.5 mm, whereas the distance between the corresponding points (rostral or caudal) of the two pairs of electrodes was 3.5 mm (2 mm wire length plus 1.5 mm between the wires). The electrodes had a very low resistance (<103 
) and a noise level of only a few microvolts (Deliagina et al. 2000).
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Implantation of the electrodes was performed in eight animals under MS-222 (Sandoz) anesthesia (100 mg/l). The plate with electrodes was implanted at the level of the third gill, through a longitudinal cut performed along the midline of the dorsal aspect of the body. The plate was positioned so that the electrodes were facing the dorsal aspect of the spinal cord (Fig. 1B). The rostral end of the plate was pushed carefully into the canal between the spinal cord and surrounding tissues to secure the electrode position in relation to the spinal cord. The wound was then closed and sutured so that the connecting wires were tightly fixed between the two sides of the wound. Vestibular and visual responses of RS neurons were tested after full recovery from anesthesia (3–4 h after implantation of the electrodes).
A unilateral labyrinthectomy (UL) was performed in six animals, usually 1 day after implantation of the electrodes as previously described in detail (Deliagina 1997a). In short, the hole was made in the dorsolateral aspect of the vestibular capsule and the labyrinth was removed with a pair of fine forceps under visual control. For a few weeks after UL, the animals were unable to maintain the dorsal side up orientation during swimming and were continuously rolling toward the damaged side (de Burlet and Versteegh 1930; Deliagina 1995, 1997a). Postmortem investigation showed that, in all cases, removal of the vestibular organ was complete. In the six animals used to study the effects of UL, vestibular responses of RS neurons were examined two times: after implantation of the electrodes and after UL. Responses were tested after full recovery from anesthesia.
Vestibular and visual stimulation
All experiments were carried out at a water temperature of 7–8°C. The lamprey was positioned in a special setup (Fig. 1C) that consisted of a tube fastened to a small platform. After having being positioned into the tube, the lamprey attached to the platform with its sucker mouth. The setup allowed us to rotate the animal in the horizontal (yaw) plane by 60° peak to peak. Two patterns of vestibular stimulation were used. First, the animal was tested during periodic sinusoidal yaw turns, at a period of 4 s (Fig. 1D). Our reason for this was to use vestibular stimuli similar to those caused by periodical head undulations during slow swimming (Islam et al. 2006a,b; Williams et al. 1989). Another stimulation pattern consisted of periodical trapezoidal turns (Fig. 1E), as if the lamprey performed sharp lateral turns when changing the direction of swimming. The transition from one position to another lasted 2 s, and each position was maintained for 4 s; the cycle duration was 12 s. Illumination of the left or the right eye was produced by two fiber-optic systems (90 W) attached to the turning platform (Fig. 1C). Because normally the resting activity in RS neurons was low or absent (see also Deliagina and Fagerstedt 2000; Pavlova and Deliagina 2002), to reveal not only excitatory but also inhibitory effects, visual stimulation was performed in combination with vestibular stimulation. This also allowed us to characterize the effects of visual input on vestibular responses. Eye illumination was usually turned off before it caused activation of the locomotor system and lateral turn (Deliagina et al. 2000). Typically, the experimental session included 50–100 tilt cycles.
Processing of data
Signals from the electrodes were amplified by conventional AC amplifiers, digitized with a sampling frequency of 10 kHz, and stored on the hard disk of an IBM AT compatible computer by means of data-acquisition software (Digidata 1200/Axoscope, Axon Instruments, Union City, CA). A representative example of the four-electrode recording of the multiunit responses to trapezoidal turns and to eye illumination is shown in Fig. 2 A.
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). 1) One of the channels was used to build primary templates and extract groups of events that matched them. The minimum percentage of points in a template was 80%, and the width of the template was roughly 20% of the spike amplitude. 2) For each of the groups, corresponding waveforms were extracted from other channels and then reclassified. Thus secondary templates were built for each group of "events" and each neuron had a set of templates (primary and secondary), one template for each channel. After that, we looked through each of the files for a given animal and piled up the templates corresponding to different neurons. In the end, common sets of templates were used to extract the activity of single neurons from all the files.
The inverse proportionality between the spike amplitude and the axon distance from the electrode allowed us to roughly estimate the laterality of individual axons in the spinal cord by comparing the amplitudes of the same spike recorded by the two rostral electrodes (Deliagina et al. 2000). The ratio (r) of minimal to maximal spike amplitude was calculated. Axons were divided into the lateral group (r 
0.4) and medial group (r > 0.4). In this paper, the laterality of the axon is used as a morphological characteristic of RS neurons (e.g., "left" neuron is the cell with the axon on the left side of the spinal cord).
To measure the conduction velocity in individual axons, a distance between the corresponding points of the rostral and caudal pairs of electrodes was divided by the time difference between the appearances of the same propagating spike in the two records. Most of the axons (106 of 138) were recorded by both rostral and caudal electrodes; all of them appeared to be descending ones. Their conduction velocity ranged from 1.6 to 4.0 m/s. In the spinal cord of the lamprey, the descending axons with such high conduction velocity belong mainly to RS neurons. The axons of the vestibulospinal neurons and lateral interneurons, which could be recorded in the area of the implanted electrodes, usually have lower conduction velocity (the range of 0.5–1.3 m/s was reported for vestibulospinal neurons by Zelenin et al. 2003; see also Bussières and Dubuc 1991; Rovainen 1979).
Figure 2A shows the mass activity in RS pathways caused by trapezoidal turns and recorded by the rostral and caudal electrodes. Five neurons with their axons on the right side of the spinal cord and five neurons with left-side axons were extracted from this record by the spike-sorting program (Fig. 2B). Identification of two of them, L4 (with medial position of the axon, r = 0.7) and R3 (with lateral position of the axon, r = 0) are illustrated in Fig. 2, C and D, respectively, where the display was synchronized by an "event" signal. One can see that, for each of the neurons, the shape and absolute value of spike waveform in individual electrodes, the ratio between the spike amplitudes in different electrodes, and the time delay between the spikes in the rostral and caudal electrodes were constant.
The activity of a population of RS neurons was presented in a form of histograms. The cycle of sinusoidal turns was divided into ten equal (0.4-s) bins (Fig. 4A) and the frequency of individual neurons was measured for a given bin and then averaged over these bins in sequential cycles and over all neurons. The cycle of trapezoidal turns was divided into six equal (2-s) bins (Fig. 4B) and the frequency of individual neurons was also averaged over sequential cycles and over neurons.
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RESULTS |
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In quiescent animals, the activity of RS neurons was very low or absent. Vestibular stimulation activated RS neurons. In eight animals, data on the activity of 138 neurons (five to 27 neurons in individual animals) were extracted from the mass activity. Based on their pattern of response to vestibular stimulation, the RS neurons were divided into four groups. Examples of vestibular responses of neurons from different groups are shown in Fig. 3 A and the relative number of neurons in different groups is given in Fig. 3B. Group 1 neurons were activated by the contralateral turn (n = 98, 71%); group 2 neurons, by the ipsilateral turn (n = 13, 9%); group 3 neurons, by both contralateral and ipsilateral turns (n = 16, 12%); and group 4 neurons showed no phasic response to turns (n = 11, 8%). Of these four groups, only the neurons of group 1 and group 2 had directionally specific vestibular responses and therefore could participate in the stabilization of orientation in the yaw plane.
The overwhelming majority of neurons belonged to group 1, both in the whole population and in individual animals (Table 1). Only in animal #7, was group 2 larger than group 1, although the number of recorded cells in this animal was very small. Group 1 was analyzed in detail. Figure 4 A shows the summary of responses of all group 1 neurons to sinusoidal turns and Fig. 4B, to trapezoidal turns. In both tests, the responses were well pronounced. In tests with sinusoidal turns, the mean value of activity during contralateral rotation (phases 0.5–1) was 2.2 ± 0.2 versus 0.4 ± 0.1 Hz during ipsilateral rotation (phases 0–0.5). In tests with trapezoidal turns, the mean value of activity in the contralateral turn (phases 0.5–1) was 1.4 ± 0.1 versus 0.2 ± 0.1 Hz in the ipsilateral turn (phases 0–0.5). The difference in both cases was statistically significant (paired t-test). In trapezoidal tests, the responses elicited by the contralateral turn decayed when a new position was maintained (Fig. 4B).
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0.4).
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In a part of the neurons, the activity was present on only one pair of electrodes; as a rule, this was the rostral pair. Responses of these neurons did not differ from those in the units identified as RS neurons and therefore they were considered together. The absence of activity of the neuron on the caudal electrodes was most likely caused by a damage of the axon by the implanted array.
Effect of unilateral labyrinthectomy on vestibular responses of group 1 neurons
Because RS neurons were normally silent before vestibular stimulation, the effect of stimulation could be roughly evaluated by simply counting the number of activated neurons. In six animals, we counted the number of active group 1 neurons both before and after UL (Fig. 6 A). The UL caused almost threefold reduction in the number of responding neurons on the side contralateral to UL (from 46 neurons in control to 16 neurons). On the side ipsilateral to UL, the number of responding group 1 neurons decreased only slightly (from 32 to 25).
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The main effects of UL—that is, a considerable reduction in the number of responding group 1 neurons (on the side contralateral to UL) and a decrease in their frequencies—were robust and observed in each of the six animals both in sinusoidal and trapezoidal tests.
Effect of unilateral eye illumination
The effect of unilateral eye illumination was studied in eight animals. Figure 2B illustrates modifications of the vestibular responses of individual RS neurons caused by left eye illumination in animal A16. The effects in individual neurons were different. The eye illumination caused an increase of activity in four left (L2–L5) and in one right (R4) group 1 neurons; in one right group 2 neuron (R5); in one left group 3 neuron (L1); and a decrease of activity in three right group 1 neurons (R1–R3). After switching off the illumination, the activity of neurons returned to the initial level.
IPSILATERAL EYE ILLUMINATION. As shown in Fig. 7 A, most of the RS neurons (n = 68, 89%) were activated by ipsilateral eye illumination, and only eight neurons (11%) were inhibited. From Fig. 7A one can also see that the majority of activated neurons (n = 51, 75%) and all inhibited neurons belonged to group 1. Ipsilateral eye illumination also activated seven neurons (10%) of group 2, three neurons (5%) of group 3, and seven neurons (10%) of group 4.
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In the population of activated neurons, the activity during both ipsi- and contrarotation increased when the eye was illuminated (compare B and C in Fig. 7). The mean value of activity during contralateral rotation (phases 0.5–1) was 3.4 ± 0.3 versus 1.8 ± 0.4 Hz in control. The mean value of activity during ipsilateral rotation (phases 0–0.5) was 1.9 ± 0.2 versus 0.2 ± 0.1 Hz in control. The difference in both cases was statistically significant (paired t-test).
In the population of inhibited neurons, the activity during contrarotation decreased when the eye was illuminated (compare D and E in Fig. 7). The mean value of activity during contralateral rotation (phases 0.5–1) was 1.5 ± 0.3 versus 3.2 ± 0.5 Hz in control. The difference was statistically significant (paired t-test). During ipsilateral rotation (phases 0–0.5) the activities during eye illumination and in control (0.4 ± 0.2 and 0.8 ± 0.2 Hz, respectively) did not differ significantly.
CONTRALATERAL EYE ILLUMINATION. The contralateral eye illumination caused inhibition in the majority of RS neurons (n = 37, 59%), excitation in 25 neurons (39%), and did not affect one neuron (2%) (Fig. 8 A). From the inhibited neurons, the majority (n = 34, 92%) belonged to group 1, one neuron (3%) to group 2, and two neurons (5%) to group 3. From the activated neurons, 13 neurons (52%) belonged to group 1, five neurons (20%) to group 2, five neurons to group 3 (20%), and two neurons (8%) to group 4. Figure 8, B–E shows frequency curves for two populations of group 1 neurons that were activated (B and C) and inhibited (D and E) by contra-eye illumination. In both populations, vestibular responses persisted during eye illumination (Fig. 8, C and E). In the population of activated neurons, the mean value of activity during contralateral rotation (phases 0.5–1) was 2.2 ± 0.3 versus 0.5 ± 0.2 Hz during ipsilateral rotation (phases 0–0.5). In the population of inhibited neurons, the mean value of activity during contralateral rotation (phases 0.5–1) was 2.0 ± 0.3 versus 0.5 ± 0.1 Hz during ipsilateral rotation (phases 0–0.5). The difference in both populations was statistically significant (paired t-test).
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In the population of inhibited neurons, the activity during contrarotation decreased when the eye was illuminated (compare D and E in Fig. 8). The mean value of activity during contralateral rotation (phases 0.5–1) was 2.0 ± 0.3 versus 3.0 ± 0.4 Hz in control. The difference was statistically significant (paired t-test).
The population of neurons (n = 25) activated by contralateral eye illumination could initiate negative phototaxis. Their conduction velocity ranged from 1.8 to 4 m/s; for 23 of them their axons were located laterally in the spinal cord.
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DISCUSSION |
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The RS neurons recorded in the present study responded to rotation in the yaw plane. To simulate head movement during undulatory swimming and sharp lateral turn, we used sinusoidal and trapezoidal turn trajectories, respectively. The RS neurons responded to both types of stimulation. All recorded neurons were classified into four groups according to their pattern of response to vestibular stimulation. The overwhelming majority of them (group 1) were activated by the contralateral yaw turn (Fig. 3). It was recently shown that the main effect of RS neurons activated by vestibular input during the contralateral yaw turn is the ipsilateral body flexion (Zelenin et al. 2005). Taken together, these findings suggest that group 1 neurons participate in the corrections of orientation in the yaw plane, by causing a turn of the animal in the direction opposite to the initial deviation (see following text).
The majority of group 1 neurons had an axonal conduction velocity of >2 m/s (Fig. 5B), which is characteristic for the large- and middle-size RS cells (Ohta and Grillner 1989; Rovainen 1967, 1978). Most of their axons were located in the lateral parts of the spinal cord (Fig. 5A). A similar distribution was found for the RS neurons responding to roll tilt (Deliagina and Fagerstedt 2000). In the distribution of pitch-related neurons, two peaks were observed: in the medial and lateral areas of the spinal cord (Pavlova and Deliagina 2002).
A small proportion of neurons activated by the ipsilateral yaw turn (group 2) could also participate in the control of yaw angle (see following text). By contrast, neurons of groups 3 and 4 did not discriminate the direction of rotation and could not directly participate in yaw control. However, the presence of tonic activity in these neurons suggests that they might affect the level of excitability in the spinal networks.
It has to be noted that the method used in the present study allowed us to record from the large- and middle-size RS neurons. These cells, however, constitute a small proportion (roughly 10%) of the whole RS population, which consists mainly of small neurons (Bussiéres 1994); vestibular responses of these small neurons remain unknown.
Origin of vestibular responses in group 1 neurons
In lampreys, a turn of the head in the yaw plane results in activation of the vestibular afferents projecting to the brain stem through the anterior branch of the contralateral vestibular nerve and through the posterior branch of the ipsilateral nerve (Lowenstein 1970; Lowenstein et al. 1968). Using electrical stimulation of individual branches, Pflieger and Dubuc (2004) showed that RS neurons are excited by the branches activated by the contralateral yaw turn and are inhibited by the branches activated by the ipsilateral yaw turn. In the present study we found that natural stimulation of vestibular organs by turns in the yaw plane results in activation of the contralateral RS neurons, confirming the functional role of vestibular projections to RS neurons revealed by Pflieger and Dubuc (2004).
To find out the relative contribution of afferents from the two labyrinths to the origin of yaw-responses in RS neurons, experiments with unilateral labyrinthectomy were performed. It was found that UL caused a significant reduction in the activity of RS neurons on the contralateral side: both the number of responding neurons and their frequency decreased. On the ipsilateral side, the number of responding neurons decreased only slightly, whereas their frequency was similar to that in control (Fig. 6). Thus for the majority of yaw-related neurons, the main source of excitatory vestibular influences was the contralateral labyrinth. These influences seem to be transmitted by the afferents in the posterior branch of the contralateral vestibular nerve (Pflieger and Dubuc 2004). Earlier it was shown that the RS neurons responding to tilts in the roll plane and to nose-up tilts in the pitch plane also receive their main vestibular input from the contralateral labyrinth (Deliagina and Pavlova 2002; Pavlova and Deliagina 2003).
Persistence of weaker vestibular responses in some RS neurons on the side contralateral to UL suggests that the excitatory input to RS neurons from the ipsilateral labyrinth supplements the main input from the contralateral labyrinth. These influences seem to be transmitted by the afferents in the anterior branch of the ipsilateral vestibular nerve (Pflieger and Dubuc 2004). Elimination of this weak ipsilateral input caused by UL is the likely reason for a slight reduction in the number of responding neurons on the side ipsilateral to UL (Fig. 6A).
Functional role of group 1 neurons
Figure 9 shows a conceptual model of the yaw control system based on the two major findings. 1) In the present study it was shown that two subpopulations of RS neurons—the right, RS(R) and the left, RS(L)—are driven by vestibular inputs (mainly from the contralateral labyrinth), so that they are activated with the contralateral yaw turn. 2) It was recently shown that the RS neurons, activated by a contralateral yaw turn, send commands to the spinal cord, which cause an ipsilateral yaw turn of the animal, that is, rotation opposing the initial turn (Zelenin et al. 2005). For example, if an external force causes passive turning of the lamprey to the left, the right subpopulation is activated by the vestibular input. This subpopulation will elicit a corrective turn of the animal to the right by the spinal mechanisms and restoration of the initial orientation in the yaw plane. Thus the yaw control system, based on vestibular reflexes, counteracts any deviations from the rectilinear swimming caused by external factors.
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). By contrast, turns in the horizontal plane do not affect the animal's orientation in relation to the gravity vector. For that reason, the yaw control mechanism receives vestibular signals only about dynamic changes of the yaw orientation, but not about the orientation itself. As a result, this mechanism can reduce rapid but not slow deviations from the swim trajectory. Thus maintenance of a certain direction of swimming in the yaw plane requires participation of other sensory inputs (e.g., visual) signaling the absolute value of the yaw angle.
In the swimming lamprey, the propulsive force is generated as a result of the periodical locomotor undulations of the head and body in the yaw plane (Wallén and Williams 1984; Williams et al. 1989). One can expect that vestibular reflexes caused by external factors and by undulatory head movements interact. Vestibular reflexes can also be rhythmically modulated by the spinal locomotor CPG by two routes: 1) the RS neurons themselves are modulated by efference copy signals (Kasicki et al. 1989) and 2) the efficacy of vestibular input to these neurons is rhythmically gated (Bussiéres and Dubuc 1992; Pflieger and Dubuc 2004). To study this problem, recording of the activity of RS neurons during swimming and correlation of this activity with active and passive head movements should be carried out.
Group 2 neurons, responding to the ipsi-turn, could supplement group 1 by activating contralateral myotomes, although these effects have not been demonstrated (Zelenin et al. 2006).
Effects of unilateral visual input
Nonpatterned visual stimuli (unilateral eye illumination) in the lamprey evoke two types of motor behavior: "negative phototaxis" and "dorsal light response." In the swimming lamprey, the negative phototaxis is a lateral turn away from the source of light (Ullén et al. 1993, 1995b, 1997). The negative phototaxis can also be observed in the lamprey attached to the bottom by its sucker mouth; it includes detachment from the substrate and a lateral turn away from the source of light, followed by the rectilinear swimming (Ullén et al. 1993, 1995b, 1997). For this type of response, the RS neurons causing lateral turn should be activated. Another type of reaction to asymmetrical eye illumination—the dorsal light response—consists of the roll tilt toward the source of light (Ullén et al. 1993, 1995b, 1997). It requires activation of RS neurons causing rolling, i.e., rotation about the longitudinal body axis.
In the present study we have identified a population of RS neurons (group 1) sensitive to turns in the yaw plane and presumably involved in the control of orientation in this plane. Can these neurons (or a part of them) be involved in the control of the negative phototaxis? It is known that visual input activates RS neurons through the neurons in the contralateral pretectum (Zompa and Dubuc 1996). They project bilaterally to RS neurons and the noncrossed projection seems to cause the negative phototaxis (Ullén et al. 1997). Thus for performing this particular function, the yaw-related RS neurons (which are known to cause the ipsilateral yaw turn; Zelenin et al. 2005) should be activated by illumination of the contralateral eye.
However, our experiments have shown that most of the group 1 neurons were excited by illumination of the ipsilateral eye and inhibited by illumination of the contralateral eye (Figs. 7 and 8). The net effect of the whole RS population would thus be not the negative but the positive phototaxis. Only a small proportion of group 1 neurons (27%) was excited by illumination of the contralateral eye, and thus they constitute the candidate neurons for mediating the negative phototaxis.
This controversy can be explained in different ways. First, one can suggest that visual input to RS neurons, observed in resting animals, is subjected to substantial modifications when the animal is in the active state, with enhancement of the connections that underlay the negative phototaxis and with inhibition of those preventing this response. In this respect it is interesting to note that, when repeatedly eliciting the responses to unilateral eye illumination, the turn away from the light was the most often observed reaction, but the turn toward the light sometimes also occurred (Ullén et al. 1995b, 1997). Second, one can suggest that there are other RS neurons, without specific reactions to yaw rotation, but nevertheless causing turns in the yaw plane. We found that some neurons activated by contralateral eye illumination had no specific responses to yaw turns (Fig. 8). They could participate in initiation of the negative phototaxis.
In the present study we argued that the majority of yaw-related RS neurons (group 1), as a consequence of specific relationships between their sensory inputs and motor effects, counteract lateral deviations of the head (caused by external destabilizing factors) and thus promote maintenance of a rectilinear swim trajectory. Does this stabilizing system also operate in the cases when the lateral turns are initiated by the lamprey itself as, say, during the negative phototaxis? Our experiments with eye illumination have shown that unilateral visual input did not change the basic pattern of responses of RS neurons to yaw turns: they were activated during the contralateral rotation (Figs. 7 and 8). These findings suggests that the yaw-stabilizing system counteracts not only passive but also active turns of the head. One can suppose that the commands for active turn, addressed to RS neurons, overcome the head-stabilizing effects of vestibular reflexes.
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: T. G. Deliagina, The Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institute, SE-17177, Stockholm, Sweden (E-mail: Tatiana.Deliagina{at}ki.se)
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ABSTRACT
INTRODUCTION
, yaw angle; FO, fiber-optic illumination system). D and E: characteristics of vestibular stimulation for sinusoidal turns (D) and trapezoidal turns (E).
