CONTROL OF LOCOMOTION IN MARINE MOLLUSK CLIONE-LIMACINA .9. NEURONAL MECHANISMS OF SPATIAL ORIENTATION

1. When swimming freely, the pteropod mollusk Clione limacina actively maintains a vertical orientation, with its head up. Any deflection from the vertical position causes a correcting motor response, i.e., bending of the tail in the opposite direction, and an additional activation of the locomotor system. Clione can stabilize not only the vertical orientation with its head up, but also the posture with its head down. The latter is observed at higher water temperature, as well as at a certain stage of hunting behavior, The postural control is absent in some forms of behavior (vertical migrations, defensive reactions, ''looping'' when hunting). The postural reflexes are driven by input from the statocysts. After removal of the statocysts, Clione was unable to maintain any definite spatial orientation. 2. Activity of the neuronal mechanisms controlling spatial orientation of Clione was studied in in vitro experiments, with the use of a preparation consisting of the CNS and statocysts. Natural stimulation (tilt of the preparation up to 90 degrees) was used to characterize responses in the statocyst receptor cells (SRCs). It was found that the SRCs depolarized and fired (10-20 Hz) when, during a tilt, they were in a position on the bottom part of the statocyst, under the statolith. Intracellular staining has shown that the SRC axons terminate in the medial area of the cerebral ganglia. Electrical connections have been found between some of the symmetrical SRCs of the left and right statocysts. 3. Gravistatic reflexes were studied by using both natural stimulation (tilt of the preparation) and electrical stimulation of SRCs. The reflex consisted of three components: 1) activation of the locomotor rhythm generator located in the pedal ganglia; this effect of SRCs is mediated by previously identified CPA1 and CPB1 interneurons that are located in the cerebral ganglia and send axons to the pedal ganglia; 2) bending the tail evoked by differential excitation and inhibition of different groups of tail muscle motor neurons; this effect is mediated by CPB3 interneurons; and 3) modification of wing movements by differential excitation and inhibition of different groups of wing motor neurons; this effect is mediated by CPB2 interneurons. 4. Gravistatic reflexes in the tail motor neurons were inhibited or reversed at a higher water temperature. 5. The SRCs are not ''pure'' gravitation sensory organs because they are subjected to strong influences from the CNS. In particular, CPC1 interneurons, participating in coordination of different aspects of the hunting behavior, exert an excitatory action on some of the SRCs, and inhibitory actions on others. It seems likely that, via these central influences on SRCs, the spatial orientation of Clione can be changed in relation to different forms of behavior.