1) Responses to eye illumination were recorded using a shallow aquarium (80 × 80 × 8 cm deep) (cf. Ullén et al. 1995a
). After being transferred to the aquarium, the animal spontaneously assumed a quiescent position, attached to the bottom of the aquarium with its sucker mouth. One eye was illuminated with an optical guide (8 mm diam, 90 W white lamp) held 1-2 cm away. The stimulus light remained on until the moment when the animal detached from the bottom of the aquarium and performed the initial turning movement. Each animal was tested repeatedly, with
60 s of dark adaptation between each test. Negative phototaxis (see Fig. 2A) was characterized by the distribution of turning angles of the initial turning movement after detachment. The roll orientation of the animal was estimated, using the position of the dorsal fins and the border between the dark back and the white belly in dorsal projection. By measuring position of the dorsal fin in relation to the left and right borders of the body, the roll angle of the animal can be estimated with a precision of ~5° at orientations near the dorsal-side-up orientation (Ullén et al. 1995b
). The DLR-A and DLR were analyzed qualitatively while the animal still remained attached and during the initial part of the locomotion, respectively (see RESULTS for further details).

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| FIG. 2.
Phototaxis in intact animals. A: quiescent lampreys, attached to bottom of aquarium with sucker mouth, responded to illumination of 1 eye with an optic guide (light) with detachment, a turning movement away from light, and locomotion. A typical trajectory is shown ( ) (interval between is 40 ms). First part of trajectory, corresponding to initial lateral turn, is indicated ( ). Turning angle of response was defined as angle between body axis of animal in initial position and trajectory of swimming with a negative sign indicating turns away from illuminated side (negative phototaxis). B: distribution of turning angles (n = 49) in all tested intact animals (n = 3). Note pronounced negative phototaxis and bimodal distribution of turning angles. In 46 out of 49 tests, a sharp turn away from light was evoked. In 3 remaining cases, sharp positive turns were seen.
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2) To analyze postural deficits during locomotion, 5-min sequences of spontaneous swimming were recorded. Earlier observations have shown that lampreys, when swimming in contact with or very near to the bottom or a wall of the aquarium, tend to swim with their ventral side turned toward the substrate, presumably by using tactile or lateral line input to stabilize their orientation (Ullén et al. 1995a
). To examine roll control when the animal was near the bottom and spontaneous yaw turns, swimming was recorded from above in the shallow aquarium. Locomotion in free water was recorded from the side in a deeper aquarium (35 × 110 × 40 cm deep). If, during the recording, the animal spontaneously attached itself to the bottom with its sucker mouth, it was stimulated to resume swimming by a gentle mechanical stimulation of the tail or sucker. Occasionally, an animal swam for a few cycles along the bottom or a wall with the sucker in direct contact with the substrate; these episodes were excluded from analysis.
Each record was first analyzed qualitatively to determine the different types of behavior displayed by the animal. Forward swimming with a dorsal-side-up orientation (<10° deviation from the vertical) was classified as normal locomotion. The number of spontaneous leftward and rightward yaw turns were counted. In some animals, spontaneous yaw turns to one or both sides were impaired: instead of turns, episodes of repeated head bending toward the lesioned side were displayed. Two types of behavior with impaired roll control were seen: continuous rolling to one side, and tilting. A tilting tendency could occur either consistently to one side or to both sides. In both cases, the animal was considered tilted when the roll angle deviated more than ~10° from the vertical. One particular pattern of behavior with impaired pitch control consisted of episodes of nearly vertical upward swimming in the water surface. In some animals, episodes of backward swimming were seen. The percentage of time spent in each behavioral category was calculated (see RESULTS).
When swimming in contact with or very near the bottom or a wall, lampreys often turn their ventral side toward the substrate (see above), presumably due to somatosensory or lateral line influences. For swimming in the deeper aquarium, the time spent in contact with the bottom therefore was analyzed separately from the time spent in free water to get separate measures of postural behavior of the animal with and without somatosensory/lateral line feedback.
The two paradigms were largely used in separate studies. Therefore, only in the case of the spinal lesions and rhombencephalic midline split were both visual responses and postural behavior during free swimming tested in the same animals.
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RESULTS |
Responses to unilateral eye illumination and postural control in control animals
Eye illumination in the intact animals evoked the DLR-A, displayed as a pronounced rotation of the body of the lamprey around the sucker, while the animal still remained attached to the bottom of the aquarium and finally detachment and negative phototaxis. With the present paradigm, the eye illumination did not have a fixed duration but terminated when the animal detached and performed the initial turning movement. The amplitude and duration of the DLR-A was therefore highly variable. If the latency for detachment and locomotion was normal (>1 s), a clear DLR-A (>10° rotation toward the illuminated side) always was seen in attached state. In many cases, the animal exhibited a roll tilt of
90° while still attached. Because of this variability in stimulus conditions and, consequently, response amplitude, the DLR-A and the DLR in the lesioned animals were compared in a qualitative manner with the response in control animals. It was not possible, with the present paradigm, to determine if the DLR-A was enhanced, and the response was only classified as present or absent. The DLR was analyzed during the first period of swimming after detachment and classified as normal if the animal, when the latency for locomotion was
1 s, displayed a clear roll tilt (>10°) after detachment but returned to normal orientation within 30 s of locomotion without rolling. If the eye illumination evoked persistent rolling around the longitudinal axis toward the illuminated side after detachment, the response was classified as enhanced. If no or an extremely weak (<10°) rotation was displayed in attached state, the response was classified as abolished or suppressed, respectively.
Figure 2A shows the trajectory of a typical locomotor response obtained with eye illumination of an intact lamprey. Characteristically, locomotion started with one sharp initial yaw turn away from light (indicated with a gray line in Fig. 2A), typically followed by approximately linear locomotion until the animal reached the wall of the aquarium. During this initial part of the response, the animal often displayed a slight roll tilt toward the stimulated side because of sustained the DLR (see above). The turning angle of the response was defined as the angle, in the horizontal plane, between the linear part of the trajectory and the body axis of the animal in the initial position (Fig. 2A). The distribution of turning angles of all responses (n = 60, 3 animals; Fig. 2B) revealed a pronounced negative phototaxis: the large majority (93%) of turns were negative (away from light), but a few sharp turns toward the light also were evoked. In Fig. 2B and similar figures, separate distributions first were generated for each animal and subsequently pooled; the bars represent means and SE of the mean. Typically, one initial negative turn was performed followed by straight swimming. The result of this initial turning movement thus, in practically all cases, was to direct the subsequent locomotion away from the light. The distribution of turning angles was bimodal in that no responses with straight locomotion or weaker turning movements were seen (Fig. 2B).
During spontaneous locomotion, intact animals (n = 4) always swam with their dorsal side up (with roll angles within ±10°), both when swimming near the bottom and in free water: no episodes of rolling or swimming with tilted orientation were observed. Spontaneous yaw turns (n = 111; 4 animals) were performed with equal probability to the left (49.6 ± 0.8%; mean ± SD) and to the right (50.4 ± 0.8%). No episodes of vertical upward swimming or backward swimming were displayed.
Ablation of the optic tectum
Tectum constitutes a major center for visuo-motor coordination, which in lamprey, as in most lower vertebrates, receives the largest optic nerve projection (Vanegas 1984
). To investigate if the studied visual responses were mediated by the tectum, five animals with bilateral tectum-ablation were tested. The typical extent of the lesion is shown in dorsal view and cross-section (midtectal level) in Fig. 3A. The optic tectum in all cases was removed completely.

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| FIG. 3.
Responses to eye illumination and postural control during spontaneous swimming in tectum-ablated animals. A: extent of tectal lesion shown schematically (shading) in dorsal view and cross-section. - - -, level of cross-section. Optic tectum was removed completely in all animals. B: enhanced negative phototaxis and dorsal light response in tectum-ablated animals. Trajectory of a typical locomotor response evoked by eye illumination is shown ( ) (interval between is 80 ms). Roll orientation of animal is shown (light line and heavy line) next to trajectory, indicating episodes when animal was swimming on side and when it was rolling around its longitudinal axis, respectively. Both negative phototaxis and dorsal light response thus were enhanced. Animal responded to eye illumination with looping due to repeated turns and rolled toward illuminated side. C: distribution of turning angles (n = 50, 3 animals). D: free swimming in shallow aquarium. Animals (n = 2) were deficient in control of their roll angle and frequently swam tilted to either side for a short period before correcting their orientation. Percentages of time spent with a dorsal side up orientation and tilted >10° are shown. E: free swimming in deep aquarium. During swimming in free water, episodes of practically vertical upward swimming were seen.
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Both negative phototaxis, the DLR-A and the DLR were retained, although altered, in the tectum-ablated animals. Negative phototaxis and the DLR were enhanced. Figure 3B shows a typical trajectory of swimming evoked by eye illumination in one of the animals. After the normal initial negative turn, repeated (often
5), horizontal turns typically were performed during the locomotor response, making the animal circle toward the nonilluminated side. Control animals, in contrast, typically performed only one initial negative turn (see above). The distribution of yaw-turning angles of the locomotor responses is shown in Fig. 3C (n = 50, 3 animals; only the first turn was considered). The DLR also was enhanced, with an increase both in amplitude and duration of the response. After detachment, the animal typically alternated between swimming with a strong roll tilt (90°) and performing complete roll turns (360°) toward the illuminated side, for >60 s. Negative phototaxis was retained in all animals. The normal termination of the responses thus was impaired after tectum-ablation.
The stabilization of roll angle under constant illumination was impaired in the tectum-ablated lampreys. During spontaneous swimming, the animals occasionally tilted to either side. A correction movement always was performed to restore the dorsal-side-up orientation but often only after several seconds. The tilts were usually <90°, but sometimes an animal tilted 180° and swam upside-down for a brief period. Figure 3E shows the time spent swimming with the dorsal side up, and the time spent with tilted orientation, for the tectum-ablated animals swimming in the shallow aquarium (n = 2). The orientation of the animal was considered tilted if the roll angle exceeded 10° in either direction. When swimming near the bottom, the animals swam tilted ~20% of the time (Fig. 3, D and E). When swimming in free water in the deeper aquarium, the postural deficit was more pronounced, presumably due to the lack of contact to the bottom, and the animals spent a roughly equal amount of time swimming tilted and with the dorsal side up (Fig. 3E). Increased postural instability in free water as compared with when swimming near the bottom was seen, not only in tectum-ablated animals, but in all lesioned animals with disturbed roll control (n = 21; P = 0.0005; Wilcoxon signed-rank test). In addition, the tectum-ablated animals displayed periods of practically vertical upward swimming at the water surface (Fig. 3E). Spontaneous yaw turns (n = 32; 2 animals) were unimpaired and performed as often toward the left (53.5 ± 5.0%) and as to the right (46.5 ± 5.0%) side.
In conclusion, the neuronal circuits for both negative phototaxis, the DLR and the DLR-A appear to be located essentially outside the tectum, although the prolonged rolling and circling after eye illumination indicates that mechanisms for the termination of both negative phototaxis and the DLR were impaired. Tectum apparently influences reticulospinal cells involved both in roll, pitch, and yaw control, because negative phototaxis and the DLR were enhanced after tectum-ablation, and the animals displayed disturbed roll and pitch control during free swimming.
Transection of the ventral tegmental commissure
The ventral tegmental commissure (Heier 1948
; Schober 1964
) contains the fibers crossing the midline in the mesencephalic basal plate, which includes the crossed tectal efferents to the reticular cells (Heier 1948
) and presumably crossed fibers from other interneurons in ventral mesencephalon (Heier 1948
). In four animals, the ventral tegmental commissure was transected (Fig. 4A). In two animals, the transection extended into the most rostral part of rhombencephalon, ending immediately rostral to the exit of the trigeminal nerve. In this way, all crossed tecto-reticular fibers were transected. These animals were tested for visual responses and showed both a retained DLR-A and enhanced negative phototaxis and DLR, like the tectum-ablated animals. The effect of the tectum-ablation thus may be, at least partly, due to a removal of crossed tecto-reticular influences. The distribution of turning angles in the animals with mesencephalic midline split is shown in Fig. 4B (n = 58, 4 animals; only the first turn was considered).

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| FIG. 4.
Phototaxis in animals with transected ventral tegmental commissure. A: extent of lesion shown schematically in dorsal view and cross-section (black bar). All fibers crossing midline in ventral mesencephalon, including crossed tectal efferents, were transected. In 2 animals, lesion extended into most rostral part of rhombencephalon (see text). B: distribution of turning angles (n = 58, 4 animals).
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Unilateral ablation of the pretectal region
The pretectum is situated immediately rostral to the optic tectum in the most caudal part of dorsal diencephalon (Kennedy and Rubinson 1977
). This region contains both cells projecting caudo-ventrally to ipsilateral and contralateral rhombencephalic reticulospinal cells (Zompa and Dubuc 1996
) and cells giving rise to crossed fibers traveling in theposterior commissure (nucleus of the posterior commissure =nucleus M1 of Schober) (Heier 1948
; Schober 1964
), but the anatomic relation of the different cell groups has not been studied. A unilateral lesion of the pretectal region was performed in eight animals. The typical extent of this lesion is shown in dorsal view and in cross-section (level of the posterior commissure) in Fig. 5A. The pretectal region in all cases was removed completely together with all axons coursing through the area. The underlying tegmentum, including the nucleus of the longitudinal fasciculus and descending fibers from the ipsilateral ventral thalamus (Heier 1948
; Schober 1964
), was left intact. In one animal, the lesion extended caudally ~200 µm into the most rostral tectum. The border between the dorsal thalamus and the pretectum is not well defined, and damage to cells in dorsal thalamus cannot be excluded. Note that the lesion also will remove all visual input to the ipsilateral optic tectum due to the transection of the optic tract (see DISCUSSION).

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| FIG. 5.
Responses to eye illumination and postural control during spontaneous swimming in unilaterally pretectum-ablated animals. A: extent of lesion shown schematically (shading) in dorsal view and cross-section. - - -, level of cross-section. Pretectal nucleus was removed completely on 1 side in all animals. B: distribution of turning angles (n = 56) in all tested animals (n = 4). Negative phototaxis and dorsal light response still could be evoked from ipsilateral eye. Contralateral eye illumination evoked no responses. C: free swimming in shallow aquarium. Animals (n = 4) usually stabilized dorsal-side-up orientation but occasionally tilted toward lesioned side. Time spent with a dorsal side up orientation and time spent tilted >10° are shown. D: free swimming in deep aquarium. When swimming in free water, a slightly increased tilting tendency and episodes with vertical upward swimming (see text) were seen.
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All responses to illumination of the contralateral eye were abolished in the pretectum-ablated animals. Single tests also were performed after 30 min of dark adaptation. From the ipsilateral eye, the DLR-A, the DLR, and negative phototaxis could be evoked. The distribution of turning angles is shown in Fig. 5B (n = 56, 4 animals). The DLR was not enhanced, except in the one animal with a minor damage also to the rostral tectum (see above), where eye illumination evoked rolling immediately after detachment.
The stabilization of roll angle was only affected in one of the four tested unilaterally pretectum-ablated lampreys. Figure 5, C and D, shows the time spent with a tilted orientation toward the lesioned side (>10°) and with the dorsal-side-up orientation in all four animals. The affected lamprey occasionally tilted
90° toward the lesioned side, more frequently when swimming in free water. The remaining three animals swam with the dorsal side up all the time (Fig. 5, C and D). Two animals displayed episodes of vertical upward swimming in the normal aquarium (Fig. 5D). Spontaneous yaw turns (n = 95; 4 animals) were performed equally well and approximately equally often toward the ipsilateral (50.5 ± 3.5%) and the contralateral side (49.5 ± 3.5%).
Hemisection of dorsal diencephalon
The results obtained on the animals with unilateral pretectum-ablation were corroborated when testing animals where the optic tract had been transected on one side (n = 4). Rostro-caudally, the lesion was performed at a middiencephalic level (Fig. 6A). Dorso-ventrally, the lesion extended approximately half-way down the brain, transecting the optic tract and thus removing optic input to the ipsilateral tectum, pretectum and probably parts of dorsal thalamus (Fig. 6A). Apart from the optic tract, the lesion also transected other fibers coursing through dorsal diencephalon. These presumably include ascending and descending connections of dorsal thalamus and the habenular region (Heier 1948
), which have not been characterized in experimental anatomic studies. The basal plate was left intact. Responses to eye illumination (n = 13; 2 animals) were abolished from the contralateral eye, whereas stimulation of the ipsilateral eye evoked the DLR-A as well as the normal DLR and negative phototaxis (Fig. 6B). As in the pretectum-ablated animals, a tendency for ipsiversive roll tilts was seen during free swimming, more pronounced in free water where episodes of vertical upward swimming also were displayed (Fig. 6, C and D; 2 animals). Spontaneous yaw turns (n = 23; 2 animals) were unimpaired and performed as often toward the ipsilateral (52.8 ± 4.0%) as to the contralateral side (47.2 ± 4.0%).

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| FIG. 6.
Responses to eye illumination and postural control during spontaneous swimming in animals with a unilateral transection of dorsal diencephalon at a middiencephalic level. A: extent of lesion shown schematically in dorsal view (black bar) and cross-section (shading). Fibers passing through diencephalic alar plate, including optic tract, were transected on 1 side, whereas ventral diencephalon was left intact. B: distribution of turning angles (n = 13) in all tested animals (n = 2). Negative phototaxis and dorsal light response still could be evoked from ipsilateral eye. As in pretectum-ablated animals, contralateral eye illumination evoked no responses. C: free swimming in shallow aquarium. Dorsal-side-up orientation usually was maintained, but occasionally lampreys (n = 2) tilted toward lesioned side. Time spent with a dorsal-side-up orientation and time spent tilted >10° are shown. D: free swimming in deep aquarium. When swimming in free water, an increased tilting tendency and episodes with vertical upward swimming (see text) were seen.
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Transection of the posterior commissure
The posterior commissure, which connects the left and the right pretectal regions (Heier 1948
; Schober 1964
), contains fibers from cell bodies in the pretectal and neighboring regions, including the dendrite of Müller cell M1 (Swain et al. 1993
). The DLR-A was present, and the DLR and negative phototaxis were normal in animals where the posterior commissure had been transected (Fig. 7A; n = 5). The distribution of turning angles is shown in Fig. 7B (n = 27, 2 animals). Postural control nevertheless was impaired in the lesioned animals. All tested animals (n = 3) had a clear tilting tendency (Fig. 7, C and D) and episodes of vertical upward swimming when swimming in free water (Fig. 7D). The animals never swam in contact with the bottom in the deeper aquarium. Spontaneous yaw turns (n = 54; 3 animals) were unimpaired and performed about equally often toward the left (52.5 ± 4.3%) or the right side (47.5 ± 4.3%).

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| FIG. 7.
Responses to eye illumination and postural control during spontaneous swimming in animals with a transection of posterior commissure. A: extent of lesion shown schematically in dorsal view and cross-section (black bar). Posterior commissure, connecting left and right pretectum, was transected completely. B: distribution of turning angles (n = 27) in all tested animals (n = 2). Negative phototaxis and dorsal light response were preserved after lesion. C: free swimming in shallow aquarium. Animals (n = 3) usually swam with dorsal side up but occasionally tilted toward either side. Time spent with a dorsal side up orientation and time spent tilted >10° are shown. D: free swimming in deep aquarium. In free water, episodes with vertical upward swimming (see text) were seen. Animals spent no time swimming in contact with bottom of aquarium.
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Roles of crossed and noncrossed pretecto-reticular projections for negative phototaxis and DLR
The contralateral optic nerve projection thus appears to play the decisive role for the DLR-A, the DLR, and negative phototaxis. The fact that the responses essentially were retained after bilateral tectum-ablation but abolished after contralateral pretectum-ablation indicates that the visual relay neurons mediating all three responses are located in the contralateral pretectal region. Cells in this region have been shown, anatomically and physiologically, to provide bilateral, mainly excitatory, projections to reticulospinal (and probably other) cells in rhombencephalon (Zompa and Dubuc 1996
). We therefore investigated the roles of the crossed and noncrossed pretecto-reticular projections for the different responses by testing animals with a hemisection at a midmesencephalic level (Fig. 8A; n = 9). Crossing pretecto-reticular fibers traverse the midline rostral to this lesion, in the commissure of the posterior tubercle (A. El Manira, M. A. Pombal, and S. Grillner, unpublished observations). The lesion thus will transect noncrossed fibers from the ipsilateral pretectum and crossed fibers from the contralateral pretectum but leave other pretecto-reticular fibers (i.e., noncrossed fibers from the contralateral prectum and crossed fibers from the ipsilateral pretectum) intact. The interpretation of the results is complicated by the fact that other pathways coursing through the mesencephalic basal plate also are transected (see DISCUSSION).

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| FIG. 8.
Responses to eye illumination and postural control during spontaneous swimming in animals with a complete hemisection at a midmesencephalic level. A: extent of lesion shown schematically in dorsal view (black bar) and cross-section (shading). Fibers passing through mesencephalon, including pretecto-reticular tracts, were transected on 1 side. B: distribution of turning angles (n = 39) in all tested animals (n = 5), with illumination of eye ipsilateral to lesion. Negative phototaxis was preserved, whereas dorsal light response was abolished. C: distribution of turning angles (n = 32) with illumination of eye contralateral to lesion. Negative phototaxis was abolished. Instead, locomotion with a turning tendency toward illuminated side was seen. D: free swimming in shallow aquarium. Animals (n = 4) had a strong rolling tendency toward intact side and only occasionally stabilized dorsal-side-up orientation. In addition, a strong tendency for yaw turns toward intact side was seen (circling; see text). Time spent with a dorsal side up orientation and time spent with continuous rolling are shown. E: free swimming in deep aquarium. When swimming in free water, animals rolled continuously toward intact side.
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Responses to illumination of the ipsilateral eye differed from responses to illumination of the contralateral eye in the hemisected animals. Illumination of the ipsilateral eye evoked normal negative phototaxis but no DLR-A or DLR. The distribution of turning angles for ipsilateral eye illumination is shown in Fig. 8B (n = 39, 5 animals). The animals frequently rolled toward the intact side during swimming (see next paragraph). The DLR-A and the DLR were abolished, but in two animals that rolled practically continuously, illumination of the eye on the lesioned side did induce a short cessation (seconds) in the rolling immediately after detachment (see DISCUSSION).
Illumination of the contralateral eye evoked an opposite picture. The DLR-A was present. Two animals rolled practically continuously toward the intact side also in symmetrical illumination, and it was impossible to determine if the DLR was enhanced. In the animals that normally rolled only episodically, however, the DLR was enhanced in that the illumination always evoked a period of rolling toward the illuminated side. The duration of the effect is impossible to estimate due to the spontaneous rolling tendency of the animals even in symmetrical illumination. The latency of the locomotor response was longer (n = 5; P = 0.0001; Mann-Whitney test) with illumination of the contralateral eye (8.1 ± 10.2 s; mean = 6.2 s) than with illumination of the ipsilateral eye (4.3 ± 5.5 s; mean = 2.0 s) or eye illumination in intact animals. Furthermore, negative phototaxis was abolished, and the initial turning movements were in the majority of cases positive, i.e., directed toward the light (n = 32, 5 animals; Fig. 8C). The crossed pretectal projection thus appears most important for the DLR, whereas the noncrossed projection presumably plays a major role for negative phototaxis (see DISCUSSION).
The animals displayed a strong rolling tendency toward the intact side (Fig. 8D). When swimming with normal orientation, the animals usually circled toward the intact side. No spontaneous yaw turns toward the lesioned side were seen. In free water, all animals rolled continuously toward the intact side (Fig. 8E). No impairment of pitch control could be detected (see DISCUSSION).
Transection of the ventral rhombencephalic commissure
The ventral rhombencephalic commissure (commissura ventralis) (Heier 1948
; Schober 1964
) contains all fibers crossing the midline in the rhombencephalic basal plate in the floor of the fourth ventricle. This includes fibers from commissural lateral line and vestibular second-order sensory neurons in the octavolateral areas in the alar plate as well as numerous cell groups in the basal plate (e.g., in the sensory and motor trigeminal nuclei) (Huard et al. 1995
). To investigate the role of crossed interaction at a rhombencephalic level for the visual responses, animals with a transection of the ventral rhombencephalic commissure (n = 2; Fig. 9A) were tested. The whole commissure was transected, from the level of the cerebellum to the obex. In this way, all fibers crossing the midline in the rhombencephalic ventral plate, including the crossed projections from second-order vestibular and lateral line sensory neurons, were transected. The DLR-A was retained, the DLR was enhanced in these animals, and eye illumination evoked rolling toward the stimulated side. The animals still responded to eye illumination with negative turns and locomotion, but the turning angles of the negative phototaxis were smaller than in control animals (P = 0.0008, Mann-Whitney test; n = 10, 2 animals; Fig. 9B). Spontaneous locomotion was slow and irregular, and the animals displayed both a deficient roll control with tilts to either side and episodes of backward swimming (Fig. 9C). One of tested animals did not perform any spontaneous yaw turns during the recording session; the other animal performed a few weak turns to either side (leftward: n = 6, rightward: n = 11). One of the animals displayed a pronounced tonic ventroflexion of the body. Both animals swam along the bottom also in the deep aquarium (not shown).

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| FIG. 9.
Responses to eye illumination and postural control during spontaneous swimming in animals with a complete rhombencephalic midline split. A: extent of lesion shown schematically in dorsal view and cross-section (black bar).- - -, level of cross-section. Fibers crossing midline in rhombencephalon, including crossed axons from vestibular and lateral line nuclei, were transected. B: distribution of turning angles (n = 4) in all tested animals (n = 2). Negative phototaxis was preserved but turning angles were smaller than normal. C: free swimming in shallow aquarium. Locomotion was weak and impaired (see text), and animals always swam along bottom even in deep aquarium (not shown). Animals displayed impaired roll control with a tilting tendency toward either side and occasional episodes of backward swimming. Time spent with forward and backward swimming (dorsal side up orientation) and time spent tilted >10° are shown.
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High spinal hemisection
To investigate the localization of fibers for roll and yaw control in the rostral spinal cord, animals with different spinal tracts transected immediately caudal to the brain stem were tested. None of these lesions affected the DLR-A, which is to be expected, because this response is performed primarily by trigeminal muscles and thus presumably does not involve spinal motor circuits (see INTRODUCTION and DISCUSSION). In animals with a complete spinal hemisection at the level of segment 1-3 (n = 4; Fig. 10A), illumination of the eye on the lesioned side evoked a normal negative phototaxis (n = 11, 4 animals; Fig. 10B) but no DLR: after detachment, the animals in all cases almost immediately assumed the dorsal-side-up orientation. This occurred also in two of the animals that had a very strong rolling tendency toward the intact side during spontaneous locomotion (in one case, rolling was continuous; see below). In all cases, the rolling ceased, and the animals swam for several seconds with the dorsal side up after the stimulation (see DISCUSSION).

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| FIG. 10.
Responses to eye illumination and postural control during spontaneous swimming in animals with a spinal hemisection performed caudal to brain stem (segment 1-3). A: extent of lesion shown schematically (shading) in cross-section. All longitudinal fibers in 1 side of spinal cord were transected. B: distribution of turning angles (n = 11) in all tested animals (n = 3) with illumination of ipsilateral eye. Negative phototaxis still could be evoked from ipsilateral eye, whereas dorsal light response was abolished. Contralateral eye illumination evoked a normal dorsal light response, but negative phototaxis was replaced with detachment and repeated head bendings without normal locomotion (see text). C: free swimming in shallow aquarium. Animals (n = 3) had a rolling tendency toward intact side. No spontaneous yaw turns toward lesioned side were seen; instead animals displayed episodes with repeated head bendings toward lesioned side. Yaw turns toward intact side were normal. Time spent with a dorsal-side-up orientation, time spent rolling toward the intact side, and time spent performing repeated head bendings toward the lesioned side are shown. D: free swimming in deep aquarium. When swimming in free water, a dramatically increased rolling tendency was seen.
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Illumination of the eye on the intact side evoked an enhanced DLR (rolling to the intact side), whereas negative phototaxis was replaced with detachment followed by repeated head bendings toward the lesioned side without locomotion. In the most rostral spinal cord, descending fibers for both roll control and yaw turns thus presumably travel predominantly on the side toward which the turn is made. At least for roll control, contralateral influences also appear to be of some importance, however (see DISCUSSION).
This was corroborated by the postural deficits displayed by the hemisected animals during spontaneous locomotion. The animals showed episodes of rolling toward the intact side, more frequently when swimming in free water (Fig. 10, C and D). Spontaneous yaw turns toward the intact side were normal, whereas no normal yaw turns were seen toward the lesioned side. Instead, spontaneous episodes of repeated head bending toward the lesioned side occurred (Fig. 10C), as after illumination of the eye on the intact side (see previous paragraph). Episodes of head bending occurred with approximately the same frequency (53.3 ± 10.5%) as spontaneous yaw turns to the intact side (46.7 ± 10.5%; total number of turns and head bendings = 65), which supports the notion that these episodes were unsuccessful attempts at performing yaw turns.
High bilateral transection of spinal lateral columns
A severe impairment of yaw turns, both spontaneous and evoked by eye illumination, was seen also after a high bilateral selective lesion to the spinal lateral columns (n = 4; Fig. 11A). In these animals, a normal negative phototaxis could not be evoked from either eye. Instead eye illumination evoked detachment and locomotion with head bendings toward the nonilluminated side (cf. above). The DLR-A was retained (see above), and the DLR was normal from both eyes. During free swimming, no spontaneous yaw turns were seen, but episodes of head bending occurred to either side with equal frequency (Fig. 11B). No deficiency in the stabilization of the dorsal side up orientation was seen. Locomotion in the animals with lateral column lesion was always relatively slow (<2 Hz) with low amplitude of the undulatory locomotor waves. When swimming in the deeper aquarium, the animals always swam along the bottom with their dorsal side up (not shown). Fibers in the lateral columns thus appear essential for the descending control of yaw turns but play a minor role for roll control. Two of the animals performed locomotor movements also when attached to the bottom with their sucker mouths, a behavior practically never seen in intact lampreys. In one of the animals, the locomotor movements persisted continually with practically the same frequency (~1 Hz).

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| FIG. 11.
Postural control during spontaneous swimming in animals with a bilateral transection of lateral columns of spinal cord performed immediately caudal to brain stem (segment 1-3). A: extent of lesion shown schematically (shading) in cross-section. All longitudinal fibers coursing in lateral columns were transected. B: free swimming in shallow aquarium. Animals swam with dorsal side up without any rolling or tilting tendencies. Locomotion was relatively weak and slow, and both leftward and rightward spontaneous yaw turns were impaired, however. Instead of normal turns, episodes of repeated head bendings to either side were displayed. Time spent with a dorsal-side-up orientation and time spent performing repeated head bendings toward left or right side are shown. Animals always swam along bottom, even in deep aquarium (not shown).
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High bilateral transection of the medial spinal cord
In animals with a bilateral lesion to the medial rostral spinal cord (n = 3; Fig. 12A), on the other hand, negative phototaxis remained intact (n = 8, 3 animals; Fig. 12B). The DLR-A was retained, whereas the DLR was abolished or suppressed. Usually no DLR was seen, but in a couple of tests, a weak remnant of the response was seen: the animal rotated a few degrees (<10°) while attached and returned to dorsal-side-up orientation within a couple of seconds after detachment. Spontaneous yaw turns (n = 121; 3 animals) were not impaired and performed approximately equally often toward the ipsilateral (49.9 ± 5.0%) or the contralateral side (50.1 ± 5.0%). The animals had a deficiency in their roll control, however, with a tendency to tilt to either side (Fig. 12C) that was more pronounced when not in contact with the bottom of the aquarium (Fig. 12D). At a rostral level, fibers for the DLR and roll control thus appear to travel mainly in the medial part of the spinal cord, unlike fibers for negative phototaxis and yaw turns.

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| FIG. 12.
Responses to eye illumination and postural control during spontaneous swimming in animals with a bilateral transection of medial spinal cord performed immediately caudal to brain stem (segment 1-3). A: extent of lesion shown schematically (shading) in cross-section. All longitudinal fibers running through medial 50% of spinal cord were transected. B: distribution of turning angles (n = 8) in all tested animals (n = 3). C: free swimming in shallow aquarium. Animals (n = 3) had a small tendency for roll tilts toward either side. Time spent with a dorsal-side-up orientation and time spent tilted >10° are shown. D: free swimming in deep aquarium. When swimming in free water, an increased tilting tendency was seen.
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DISCUSSION |
Pathways for visual postural reflexes
Putative central pathways for visual postural reflexes in lamprey are shown in Fig. 13A, which summarizes the results of the following lesion experiments. Contralateral transection of the optic tract at the middiencephalic level by hemisection of dorsal diencephalon (lesion 1co, Figs. 1B and 6A), or contralateral ablation of the pretectal region (lesion 2co, Figs. 1B and 5A), abolished the DLR and the DLR-A. Both behaviors were normal after the same lesions on the ipsilateral side. The contralateral optic nerve projection thus appears necessary and sufficient for the DLR and the DLR-A in lamprey. This is in accordance with the view of Ward et al. (1995)
that ipsilateral visual projections in noneutherian species in general are functionally neutral.

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| FIG. 13.
Pathways demonstrated to be of importance for dorsal light response and negative phototaxis. A: pathways for dorsal light response. Neurons in contralateral pretectum are necessary and sufficient for dorsal light response. Major secondary projection is formed by excitatory commissural pretectal cells, contacting reticulospinal cells, which in turn predominantly excite ipsilateral spinal premotor and motor neurons. Earlier studies indicate that MRRN plays a major role for roll control (see text). Noncrossed inhibitory pretecto-reticular influences also may play a role for the dorsal light response (see text). B: main pathway for negative phototaxis. As for dorsal light response, neurons in contralateral pretectum are necessary and sufficient for negative phototaxis. Noncrossed descending pretectal influences play major role for generation of negative turn and initiation of locomotion.
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Bilateral tectum-ablation (lesion 6, Figs. 1B and 3A) did not abolish the DLR nor the DLR-A; the DLR even was enhanced after the lesion. This supports the view that the basic circuitry for the DLR is extra-tectal as in goldfish (Watanabe et al. 1995
; Yanagihara et al. 1993a
,b
) and carp (Mori 1993
), but the enhancement of the response, with prolonged tilting and rolling, shows that the normal time course and termination of the DLR was impaired. Generally, the tectum appears less involved in postural control than in behaviors such as orientation and avoidance responses, which require an analysis of patterned visual stimuli at particular locations in external space (Dean et al. 1989
; Ewert 1987
; Masino 1992
; Vanegas 1984
). The enhancement of the DLR seen after tectum-ablation shows that the tectum directly or indirectly can influence the roll control system, however. One explanation for this enhancement could be that the tectum, when intact, inhibits the extratectal visual influences to the roll control system, perhaps at a pretectal level or within the reticular nuclei themselves. An increase of excitability in reticular cells was observed in vitro after removal of the tectum (Deliagina et al. 1993
). The DLR was enhanced also in animals with a transection of the ventral tegmental commissure (lesion 4, Figs. 1B and 4A) where the crossed tectal efferents traverse the midline. This finding suggests that the effect of tectum-ablation is largely due to removed crossed tecto-reticular influences.
The fact that the DLR and the DLR-A persisted after tectum-ablation (lesion 6, Figs. 1B and 3A) and the fact that both responses were abolished by denervation (lesion 1co, Figs. 1B and 6A) or ablation (lesion 2co, Figs. 1B and 5A) of the contralateral pretectum taken together strongly suggest that the visual relay neurons mediating the DLR and the DLR-A are located in the contralateral pretectal region. The rostral and caudal borders of the pretectum are defined poorly in the lamprey, however (see RESULTS). It is possible that the contralateral pretectum-ablation (Fig. 5A) also damaged some dorsal thalamic neurons or some rostral tectal cells; this could contribute to the motor deficits in the pretectum-ablated animals. The possibility that the visual projection to contralateral mesencephalic tegmentum and putative minor optic fiber contacts with ventral thalamic neurons (A. El Manira, M. A. Pombal, and S. Grillner, unpublished observations) also play a minor role for the DLR and the DLR-A can likewise not be completely ruled out.
The posterior commissure connects the left and right pretectal regions (Heier 1948
). The fact that the DLR and the DLR-A were retained in animals with transected posterior commissure (lesion 3, Figs. 1A and 7A) suggests that interaction between neurons in the left and right pretectal regions is not crucial for the responses.
Ablation of the pretectum has been reported to abolish the DLR also in goldfish (Watanabe et al. 1995
; Yanagihara et al. 1993a
,b
) and carp (Mori 1993
). In higher vertebrates, pretectal nuclei also have been shown to be involved in visual postural reflexes, in particular optokinetic responses in the horizontal plane (Fan et al. 1995
; Fite 1985
; Simpson 1984
).
The reticulospinal system plays a prominent role in the control of the DLR (Deliagina 1995
; Deliagina et al. 1993
; Ullén et al. 1996
). In vitro experiments have shown that visual input excites reticulospinal neurons. An asymmetrical activation of predominantly ipsilateral cells was seen mainly in the medial rhombencephalic reticular nucleus (MRRN) (Deliagina et al. 1993
; Ullén et al. 1996
). Zompa and Dubuc (1996)
have demonstrated that cells in the pretectal region excite MRRN cells and cells in the posterior rhombencephalic reticular nucleus (PRRN) bilaterally through crossed and noncrossed projections (Fig. 1A). The crossed pretectal efferents traverse the midline in the commissure of the posterior tubercle in ventral diencephalon (A. El Manira, M. A. Pombal, and S. Grillner, unpublished observations). The visually evoked excitation of ipsilateral MRRN cells, underlying the DLR, thus could be mediated both directly by the crossed excitatory pretecto-reticular pathway or indirectly through noncrossed pretectal projections to interneurons, which, in turn, cross the midline more caudally in mesencephalon or rhombencephalon. That the crossed pretecto-reticular projection plays the decisive role for the DLR is supported by two main observations in the present study: ipsilateral mesencephalic hemisection (lesion 5i, Figs. 1B and 8A), which transects the crossed fibers from the contralateral pretectum but leaves the noncrossed ones intact, abolished the DLR as well as the DLR-A. Contralateral mesencephalic hemisection (lesion 5co, Figs. 1B and 8A), on the other hand, did not affect the DLR, nor the DLR-A. In addition, the DLR was retained, and even enhanced, both in animals with transection of the ventral tegmental commissure (lesion 4, Figs. 1B and 4A) and in animals withcomplete rhombencephalic midline split (lesion 7, Figs. 1B and 9A).
Optic nerve stimulation in vitro also inhibits contralateral MRRN cells (Ullén et al. 1996
) (see INTRODUCTION). The findings in the present study give support for that this inhibitory input could contribute to the DLR in vivo. Some of the animals with mesencephalic (lesion 5, Figs. 1B and 8xA) or spinal hemisection (Fig. 10A) rolled continuously toward the intact side. In these animals, illumination of the eye on the lesioned side caused a short pause in the rolling. The simplest explanation for these findings is that MRRN neurons on the intact side were inhibited by the stimulation. This inhibition may be provided by inhibitory noncrossed pretectal efferents, which have been demonstrated to provide direct input to some MRRN cells (Zompa and Dubuc 1996
) (Fig. 13).
The pathway for the DLR in the upper spinal cord was traced by partial transections. Ipsilateral hemisection (Fig. 10A) abolished the DLR, whereas contralateral hemisection did not. After bilateral transection of the lateral columns (Fig. 11A), the DLR remained normal, whereas the response was suppressed or abolished after transection of the medial spinal cord (Fig. 12A). Rostrally, fibers for the DLR thus appear to travel mainly in the medial ipsilateral spinal cord (Fig. 13). According to known anatomic data, the medial spinal cord carries most of the fibers from MRRN, the anterior rhombencephalic reticular nucleus and the mesencephalic reticular nucleus, but only a minority of the PRRN axons (Bussières 1994
). The present study is thus in accordance with earlier results, which indicate that MRRN rather than PRRN plays a major role for the DLR (Deliagina et al. 1993
). The DLR-A was unaffected by the spinal lesions.
Whereas the DLR is mediated by reticulospinal neurons, which influence spinal motor circuits, the DLR-A is performed by trigeminal muscles rotating the body around the sucker mouth (see INTRODUCTION). The present study indicates that both responses share a common pathway through the contralateral pretectum. Also in mesencephalon, fibers for the DLR-A appear to follow the same pathway as fibers for the DLR, because the contralateral mesencephalic hemisection (lesion 5co, Fig. 1B) did not abolish either response, whereas both responses disappeared after ipsilateral hemisection (lesion 5i, Fig. 1B). How visual signals related to the DLR-A finally reach the trigeminal motor nucleus is not known. It is noteworthy that both the DLR and the DLR-A are sustained, i.e., a tilted orientation is maintained after cessation of the visual stimulation. One possibility would be that rhombencephalic reticular cells are involved in both responses and that the DLR-A, as well as the DLR, can be viewed as a consequence of a shift in the set-point of the roll control system (Deliagina 1995
; Deliagina et al. 1993
; Grillner et al. 1995
).
Pathways for negative phototaxis
Figure 13B shows putative central pathways for negative phototaxis in lamprey. The figure summarizes results of the following lesion experiments. Bilateral tectum-ablation (lesion 6, Figs. 1B and 3A) or transection of the ventral tegmental commissure (lesion 4, Figs. 1B and 4) enhanced negative phototaxis. It is notable that, although the tectum receives the largest optic nerve projection, it thus appears not to play an essential role for negative phototaxis. Contralateral ablation (lesion 2co, Figs. 1B and 5A) or denervation (lesion 1co, Figs. 1B and 6A) of the pretectal region, on the other hand, abolished negative phototaxis. The response was normal after the same lesions were performed on the ipsilateral side (lesions 1i and 2i, Fig. 1B). Transection of the posterior commissure did not affect negative phototaxis (Fig. 7). The data taken together thus strongly supports that the contralateral optic nerve projection is sufficient and necessary for negative phototaxis and suggests that the involved relay neurons, as for the DLR and the DLR-A, are located primarily in the contralateral pretectal region with possible contributions of dorsal thalamic and rostral tectal cells.
The enhancement of negative phototaxis after tectum-ablation could be due to disinhibition of pretectal or reticulospinal cells involved in yaw control. Increased reticular responsiveness to visual stimuli has been observed after removal of the tectum (T. G. Deliagina, unpublished observations). The tectum thus can affect reticulospinal cells involved in yaw control, and it appears likely that the tectum in lamprey also is involved in more complex motor acts, such as orientation movements. The pretectum/posterior thalamus plays an important role for visual avoidance responses also in the toad and other amphibians: pretectal stimulation evokes avoidance behaviors such as ipsiversive turning, ducking and backward movements, and lesions to the pretectum impair or abolish the avoidance of visual threat, at least acutely (for review, see e.g., Ewert 1987
).
The data obtained in the present study are not conclusive with regard to the specific roles of the crossed and noncrossed pretecto-reticular projections for negative phototaxis. The experiments on animals with mesencephalic hemisection (Fig. 8) show that either projection alone is enough to mediate visually evoked activation of locomotion. In the intact animal, both pathways thus presumably contribute significantly to the initiation of swimming. Three findings in these animals give some support for the hypothesis that the noncrossed projection is the most important one for negative phototaxis, however, as listed below.
1) Locomotion latencies were shorter with illumination of the eye on the lesioned side than with illumination of the eye on the intact side. This indicates that the noncrossed pretecto-reticular projection provides a stronger excitation of the reticulospinal cells involved in initiation of locomotion.
2) Negative turns were only evoked with illumination of the eye on the lesioned side. This suggests that the noncrossed pretecto-reticular projection provides the bias of activity in contralateral reticulospinal cells that is necessary for the negative turn. This finding obviously has to be interpreted with some caution, however. Any asymmetry in the activity of reticulospinal cells involved in the initiation of locomotion or yaw control is likely to produce lateral turning movements. It is notable, that with illumination of either eye, turns always were directed toward the nonlesioned side, presumably due to a general increase of excitability in reticular cells on the nonlesioned side caused by the lesion. The fact that illumination of the eye on the lesioned side evoked negative turns and locomotion thus does not in itself imply that the circuitry for normal negative phototaxis was intact.
3) Negative phototaxis was retained both in animals with transection of the ventral tegmental commissure (Fig. 4) and in animals with transection of the ventral rhombencephalic commissure (Fig. 9). This excludes the possibility that interneuronal fibers crossing the midline caudal to diencephalon are essential to provide the excitation of contralateral reticulospinal cells necessary for the negative turn. Such fibers would have to play an important role for negative phototaxis, if the bias in activity were induced indirectly by the crossed pretectal projection.
In any case, the neural correlates of negative phototaxis are likely to be more complicated than for the DLR, where basic aspects of the response can be explained by just assuming that the pretectum relays an asymmetrical input signal further to the MRRN neurons. The bimodal distribution of turning angles in negative phototaxis (Fig. 2B) is noteworthy. One explanation for this could be that the initial turning movement is produced by a special neuronal circuit for the generation of sharp turns, which is triggered merely by the stimulation. In most cases, the turns were directed away from light but, under some circumstances, sharp turns toward the light were produced instead. In animals with transected ventral rhombencephalic commissure (Fig. 9), turning angles of both visually evoked negative turns and spontaneous yaw turns were smaller than normal. A possibility is that bilateral interaction at a rhombencephalic level plays a role for the generation of sharp horizontal turns.
In animals with spinal hemisection, illumination of the eye on the intact side evoked no negative phototaxis but repeated contraversive bendings of the head. This corroborates earlier studies, which showed that descending signals for yaw turns travel in the ipsilateral side of the spinal cord (McClellan 1988
). The head bendings probably occur because of repeated failed attempts to perform a negative turn; the turning wave can apparently not be propagated across the lesion. Bilateral transection of the lateral columns of the spinal cord impaired negative phototaxis bilaterally, whereas the response was retained after a transection of the medial spinal cord. In the rostral spinal cord, descending fibers for yaw control and initiation of locomotion thus appear to travel mainly in the lateral columns (McClellan 1988
) (Fig. 13). Anatomic studies have shown that the lateral columns carry the majority of fibers from PRRN (Bussières 1994
; see above), and the data in the present study thus supports the view that PRRN plays an important role for yaw control and initiation of locomotion.
Postural deficits in the lesioned animals
The stabilization of roll angle in the tectum-ablated lampreys was deficient in that the animals showed an increased tendency for larger roll tilts in either direction (Fig. 3). Furthermore, the amplitude and duration of the DLR was increased after tectum-ablation. In the light of comparative data on tectal motor functions, it appears likely that the tectum is not directly involved in the stabilization of roll angle (Masino 1992
; Vanegas 1984
). Postural deficits could occur anyway after tectum-ablation because of changes in excitability of reticulospinal neurons, which serve as common target neurons for both postural and other motor systems in the lamprey brain. Removed tectal input to other extra-tectal structures, e.g., the pretectum, also could contribute to the postural instability. The tilting tendency was larger when the animal was swimming in free water than when it was in contact with the bottom. This was a general feature of all lesioned animals with a disturbance to the roll control system and presumably reflects the lack of somatosensory postural reflexes, and perhaps weaker lateral line input, when the animal was not in contact with the substrate.
An interesting behavior in the tectum-ablated animals is the episodes of vertical upward swimming. The same disturbance of the pitch control system is displayed also by blinded animals (Ullén et al. 1995b
). Upward turns are performed by dorsiflexions of the body. The vertical upward swimming episodes could occur because of removal of visual excitatory influences on the ventral myotomes. Removing vestibular input by labyrinthectomy (Ullén et al. 1995a
) or rhombencephalic midline split, on the other hand, induces a tonic ventroflexion of the body. It thus appears that the visual and vestibular systems in lamprey predominantly excite ventral and dorsal myotomes, respectively. It should be noted, however, that the rhombencephalic midline split transects all fibers crossing the midline in the ventral rhombencephalic commissure, which also includes e.g., secondary lateral line fibers.
Unilaterally pretectum-ablated lampreys (Fig. 5) and animals with a unilateral transection of dorsal diencephalon, including the fibers of the optic tract (Fig. 6), displayed a small tilting tendency toward the lesioned side. A similar tilting tendency toward the side with an intact eye is seen in animals with one removed eye (Ullén et al. 1995b
). The explanation is most likely an asymmetry in the roll control system due to unilateral removal of tonic visual input. Yaw turns were performed equally well to both sides. If the circuitry for generation of spontaneous yaw turns and the negative yaw turn in negative phototaxis is common, it is thus in any case not located in the pretectum. In free water, episodes of vertical upward swimming were seen, most likely due to removal of visual input to ventral myotomes (see previous paragraph). Such episodes, and an increased roll tilt tendency to either side, also were displayed by animals with posterior commissure transection (Fig. 7). The observed deficits thus probably occur partly because of disturbed pretectal functions.
Hemisection at a midmesencephalic level (Fig. 8) induced a strong rolling and circling tendency toward the intact side. At a mesencephalic level, descending steering control fibers thus carry signals mainly for ipsiversive turns both in the transversal and the horizontal planes. This is also in accordance with the data on visual responses.
The animals with rhombencephalic midline split (Fig. 9) showed severe motor deficits and poor locomotion presumably because of the complete elimination of crossed vestibular and lateral line influences to the reticulospinal cells and spinal cord. The observed roll tilting tendency can be attributed to the missing vestibular input. In addition, the animals displayed episodes of continuous backward swimming. This behavior also is displayed by labyrinthectomized animals (Ullén et al. 1995a
), and a possible explanation is that the crossed vestibulospinal tract, which in lamprey projects only to the rostral spinal cord (Rovainen 1979
), normally contributes to an increased excitability of the rostral segments; this presumably plays a important role to induce the rostro-caudal phase lag necessary for forward swimming (Matsushima and Grillner 1992
).
The postural deficits displayed by the animals with rostral transections to different spinal tracts confirm the result of McClellan (1988)
, that fibers for yaw turns travel mainly in the lateral columns. Complete rostral spinal hemisection impaired all yaw turns toward the lesioned side and induced a strong rolling and circling tendency toward the intact side. Transection of the lateral columns impaired yaw turns but did not cause any detectable defects in roll control. Locomotion in these animals was very slow, however, and always along the bottom of the aquarium so that postural control in free water could not be evaluated. It is noteworthy that two of the animals displayed continuous locomotor movements even when attached with their sucker mouths, which indicates that the excitability of the spinal cord was increased. This was not reported by McClellan (1988)
, who studied a large number of lampreys with lesions to the lateral spinal cord and found that the majority of animals were unable to initiate locomotion. The most likely explanation for the discrepancy is that the transection used by McClellan was slightly larger than in the present study, including both lateral and intermediate parts of the spinal cord: in cases where the intermediate parts of the cord were spared, McClellan (1988)
also found that locomotion could be initiated. Roll control fibers were found to course mainly in the medial spinal cord. Animals with transected medial spinal cord showed an increased tilting tendency in particular when swimming in free water.