Neurobiology of the scallop. I. Starfish-mediated escape behaviours

(i) In the scallop Pecten ziczac , escape responses triggered by the chemosensory stimulus of a starfish are highly stereotyped and reproducible. These responses are characterized either as jumps, i. e. single, rapid valve closures, or as swims consisting of a rapid sequence of valve closures. Jumps are evoked by a starfish stimulus to the lateral and ventral mantle edges, regions innervated by pallial nerves extending from the parietovisceral ganglion. Swimming is triggered specifically by a stimulus at or near the dorsal ‘ears’ of the shell, regions innervated by pallial nerves from the cerebral ganglion. (ii) Escape responses begin with a characteristic gaping of the valves. Evidence from simultaneous recordings of shell movement, and from electrical activity in the smooth muscle and its efferent nerve, has demonstrated that the relaxation of the smooth adductor muscle responsible for valve gape is an active process mediated by efferent discharges from the parietovisceral ganglion. Sustained valve adductions evoked by direct electrical stimulation of the smooth muscle can also be voluntarily relaxed by efferent control. The ‘resting’ tension of the smooth muscle that normally maintains the partially adducted ( ca . 50 %) shell posture is not a result of tonic efferent activity. Denervation of the smooth muscle eliminates the opening phase of escape responses and all other slow valve adductions. The resulting shell posture, however, is equivalent to that maintained normally by the intact scallop during periods of inactivity. Swim responses in the smooth muscle-denervated scallop passively reset the smooth muscle to shorter lengths. The valves then gradually reopen, due to the force of the compressed hinge resilium, although at a much slower rate than typically occurs in the intact scallop. These results indicate that the smooth muscle normally exists in a ‘catch ’ state, and that catch must be actively released during swimming and at the beginning of an escape response. (iii) Contraction of the smooth adductor muscle is timed closely with that of the striated muscle in the jump response, but is delayed until the end of the swim cycle. As a result, all escape behaviours terminate with a slow reopening of the valves due to the slow relaxation properties of the smooth muscle. Repetitive swim-like responses can be evoked under a variety of experimental circumstances that would eliminate feedback from putative stretch receptors in the adductor muscle. Rapid jump and swim adductions are therefore not due to stretch receptor feedback upon motor nerves innervating the striated muscle, and jumps and swims are not terminated as a result of sustained adductions, which would interrupt a stretch receptor reflex cycle. (iv) Escape by swimming is the result of a central motor programme, the behavioural expression of which depends on the site of peripheral chemosensory stimulation. This programme coordinates excitatory efferent activity in the smooth and striated adductor muscles, in addition to efferent control of smooth muscle catch and relaxation. Transection of the cerebrovisceral connectives eliminates all repetitive swimming activity and blocks relaxation of the smooth muscle; only jumps remain. There­fore, although the efferent nerves, and presumably their oscillatory activity, originate in the parietovisceral ganglion, the high-level control of escape behaviour resides in the cerebral ganglion.