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First published online December 3, 2004
Journal of Experimental Biology 207, 4595-4603 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.6247

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Vestibular compensation in lampreys: restoration of symmetry in reticulospinal commands

Elena L. Pavlova¹, Lyudmila B. Popova², Grigori N. Orlovsky¹ and Tatiana G. Deliagina^1,*

¹ The Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institute, SE-171 77, Stockholm, Sweden
² A. N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow 119899, Russia

View larger version (44K): [in a new window]   Fig. 1. (A) Positioning of electrodes for recording the activity in RS pathways. One array (electrodes 1 and 2) was implanted at the level of the third gill, and the other array (electrodes 3–6) 20–30 mm more caudally. (B) Arrangement for recording vestibular responses in RS neurons. The lamprey was positioned in the tube and rotated around its longitudinal axis (, roll tilt angle). (C) A representative example of vestibular responses in RS pathways and individual RS axons in the animal compensated after the left unilateral labyrinthectomy (UL). Two sequential full turns (clockwise and counterclockwise) were performed in 45° steps. Shaded rectangles indicate the normal (horizontal) orientation of the animal. Positions of the animal in successive steps (in relation to the direction of gravity force) are shown. The left half of the lamprey body is shaded. Vestibular responses were measured separately for each of the three intervals of a step (inset); the activity in interval 1 (during rotation) will be considered as a dynamic response, the activity in intervals 2 and 3, as early and late static responses, respectively. Traces E1 and E2 show the mass activity in RS pathways recorded by the left and right electrodes of the rostral array, respectively (electrodes 1 and 2 in A). Seven neurons were separated from the mass activity using the spike-sorting program. The neurons L1–L3 had their axons located on the left, ipsilateral to the UL side of the spinal cord (i-UL group). The neurons R1-R4 had their axons located on the right, contralateral to the UL side (co-UL group).

View larger version (47K): [in a new window]   Fig. 2. Summary of responsesto full turn rotation in RS neurons of compensated UL-animals, tested in light. (Ai,Aii) Number of active neurons as a function of the roll angle. This value was calculated as the number of neurons activated in each angular step in each of the animals, and then averaged over all six animals. (Bi,Bii) Average discharge frequency of neurons as a function of roll angle. This value was calculated as the number of spikes per second generated by each neuron in each step and then averaged over all active neurons in the group (N=31 and 30 for Bi and Bii, respectively). The 0° angle corresponds to the dorsal-side-up orientation of the lamprey. The angular zones where the ipsilateral (i) or contralateral (co) labyrinth was facing downward are indicated. Rotation was performed towards the contralateral labyrinth in turn a, and towards the ipsilateral one in turn b. Each step of rotation was divided into three intervals, and responses were calculated separately for each interval (see inset and legend in Fig. 1). In each of the steps, the dynamic response (activity during rotation) is shown by a black bar, the early and late static responses are shown by two successive shaded bars. Values are means ± S.E.M.

View larger version (45K): [in a new window]   Fig. 3. Summary of responses to full turn rotation in RS neurons of compensated UL-animals tested in darkness. (Ai,Aii) Number of active neurons as a function of roll angle. (Bi,Bii) Average discharge frequency of neurons as a function of roll angle (N=14 and 12 for Bi and Bii, respectively). Designations as in Fig. 2.

View larger version (26K): [in a new window]   Fig. 4. Schematic outline of the impairment of the postural system caused by UL, and restoration of postural function in compensated lampreys. (A) Conceptual model of the roll control system as proposed previously (Deliagina and Pavlova, 2002). Left and right groups of RS neurons, RS(L) and RS(R), receive vestibular (V) and visual (E) sensory inputs. The plus and minus signs without parentheses indicate the major effects on RS neurons produced by these inputs, the signs in parentheses indicate the minor effects. Weaker inputs from the ipsilateral labyrinths are shown by dotted lines. The presumed directions of rolling caused by RS(L) and RS(R) are indicated by the white and black arrows, respectively. (B–D) Operation of the model under different conditions. The curves represent the activity of the left and right groups of RS neurons as a function of roll angle. (B) Control (intact lamprey). The two activity curves intersect, and the system has an equilibrium point at 0° (dorsal-side-up orientation). (C) The right labyrinth removed (shown by a shaded rectangle in A). The system has no equilibrium point. (D) The result of vestibular compensation. Plastic changes in the postural network caused a restoration of vestibular responses in RS(L) neurons (as a result of augmentation of input from the ipsilateral labyrinth) and recreation of the equilibrium point.