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The pattern of motor coordination underlying the roll in the lamprey

Pavel V. Zelenin^*, Sten Grillner, Grigori N. Orlovsky and Tatiana G. Deliagina

The Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institute, SE-171 77, Stockholm, Sweden

View larger version (23K): [in a new window]   Fig. 1. (A) Experimental arrangement. The side view and view from above, seen in the mirror, of the swimming lamprey were video recorded. (B) Processing of video images. The body outlines in the frontal (top) and sagittal (bottom) planes obtained from the frame in which the animal was positioned with its back up. The position of the gills is shown in the side view. The body midline is marked by 21 circles located equidistantly along the `body length' axis (x), where anterior = 0% and posterior = 100%. The body shape was approximated by circles drawn though each of three neighboring midline points. The arcs of the circles for one of the points are shown together with their radii, Ry and Rz, for the frontal and sagittal planes, respectively. (C) The inverse of the circle radius characterizes the curvature at a given point of the body. The curvature was plotted in coordinates x (`body length') versus 1/Rz (curvature in the sagittal plane), x (`body length') versus 1/Ry (curvature in the frontal plane), and 1/Ry (curvature in the frontal plane) versus 1/Rz (curvature in the sagittal plane). The last plot provides information about coordination of flexions in the sagittal and frontal plane. In these and all following plots, the units for the x axis are percent of body length, while those for the 1/Ry and 1/Ry axes are arbitrary units inverse to the x units. The scales for 1/Ry and 1/Rz axes are always the same.

View larger version (40K): [in a new window]   Fig. 6. An example of roll turn performed by a lamprey with left hemisection of the spinal cord. (A,B) Side and top views for 30 consecutive frames. The level of hemisection is indicated in frame 1 (arrows). (C–E) The curvature plots for selected frames analogous to those used in Fig. 2. The roll turn is performed in steps. In frames 1, 12 and 25, the animal starts rolling to the right (start 1, 2 and 3). In frames 9, 19 the rolling decelerates (stop 1, 2). Data for the start moments are shown in red, and for the stop moments in blue. Note that in E most of the data points for the start moments are located in right ventral and left dorsal quadrants, and most of those for stop moments are located in left ventral and right dorsal quadrants, i.e. similar to Fig. 3E. R, right; L, left; D, dorsal; V, ventral sides of the body.

View larger version (34K): [in a new window]   Fig. 2. Normal horizontal swimming of an intact lamprey with its dorsal side up. Nine consecutive frames are shown. (A) Side view, (B) top view of the lamprey. The frames in A and B are stacked, with no forward movement indicated. (C) Body flexions in the sagittal plane. (D) Body flexions in the frontal plane. (E) The curvature data presented in the transverse plane. Data points corresponding to the same frame are connected with lines. The points and lines for all 9 frames are superimposed.

View larger version (27K): [in a new window]   Fig. 3. Corrective roll turn performed by an intact animal. (A,B) The side and top views for 18 consecutive frames. (C–E) Curvature plots for frames 2 (red), 13 (blue) and 17 (green) are analogous to those in Fig. 2. In frame 2, the animal is positioned with its right side up and starts rolling to the right. In frame 13, the animal has almost reached the dorsal-side-up position. In frame 18, the animal is positioned with its dorsal side up and its body is straightened in the sagittal plane; this shape is similar to that during normal swimming. Note that in E all data points for frame 2 are situated in right ventral and left dorsal quadrants and that most of the data points for frame 13 are located in left ventral and right dorsal quadrants. On the other hand most of the data points for frame 18 are located close to the abscissa, as seen during undisturbed swimming. R, right; L, left; D, dorsal; V, ventral sides of the body. White dots in frames 13-18 are the white markers attached to the skin along the dorsal midline.

View larger version (22K): [in a new window]   Fig. 7. Conceptual model of the roll postural system. (A) Right and left groups of reticulospinal (RS) neurons, RS(R) and RS(L), receive inputs from the labyrinths (La); they affect the spinal networks to evoke oblique body flexions (double-headed arrows) that lead to rolling of the lamprey. (B) Operation of the system. The curves represent the activity in RS(R) (thick line) and RS(L) (thin line) as a function of roll angle. Vestibular input causes activation of RS(R) and RS(L) with the contralateral tilt. Directions of rolling caused by RS(R) and RS(L) are indicated by the black and white arrows, respectively. The system has an equilibrium point at 0° (dorsal-side-up orientation). (C) Sequence of events during restoration of normal orientation by the lamprey, following an imposed 90° tilt to the left (see text for details). Thick arrows in iii and iv indicate the direction of the roll turn. R, right; L, left; D, dorsal; V, ventral sides of the body.

View larger version (17K): [in a new window]   Fig. 4. An episode of swimming performed with a stable orientation of left side up, with a load attached to the back of the lamprey (shown as a white rectangle in A). (A,B) The side and top views in eight consecutive frames are analogous to those illustrated in Fig. 2. (C) The curvature plots for body configurations in the transverse plane for frames 2, 5 and 8 are presented and are analogous to the plots in Fig. 3E. R, right; L, left; D, dorsal; V, ventral sides of the body.

View larger version (35K): [in a new window]   Fig. 5. An example of corrective roll turn performed by a spinalized animal. (A,B) The side and top views in twelve consecutive frames are analogous to those in Fig. 2.(C–E) The curvature plots in the transverse plane for frames 4, 8 and 12; they are analogous to frames 3, 13 and 18 in Fig. 3: rolling accelerates, rolling decelerates, body is straightened. In frame 4, the level of spinalization is indicated with arrows; the part of the body caudal to the spinalization site is shown in grey. The curvature graph for the body part rostral to the spinalization level is shown with solid lines, while that for the part caudal to the spinalization is shown with broken lines. R, right; L, left; D, dorsal; V, ventral sides of the body. White dots in A and B are the white markers attached to the skin along the dorsal midline.