Cranial components of startle behavior in larval and adult lampreys

Abstract

Larval lampreys ( Petromyzon marinus) exhibit a combination of cranial reflexes during their vibration-evoked startle response, including strong contractions of the gill chamber, velum and oral hood. These reflexes were confirmed by applying brief vibratory stimuli to an otic capsule and recording movement and electromyograms in moving preparations and efferent cranial nerve activity in curarized preparations. Vibration elicited efferent discharge in cranial nerves V, IX and X on both sides. The responses were lost following labyrinthectomy. The larval startle response results in water from the contracting gill chamber being expelled through the mouth and temporarily reduces head width. Reduced head width may facilitate the rapid withdrawal which is observed during startle behavior in burrowed larvae [ S. Currie (1985) Neurosci. Abstr. 11, 268; S. Currie and R.C. Carlsen J. exp. Biol. (in Press)]. Adult lampreys ( Entosphenus tridentata) attached to the wall of an aquarium by their suctorial disc, exhibited a brief but intense suction increase following a vibratory stimulus initiated by a tap to the aquarium wall. Oral suction (negative pressure) ranged from −0.6 to −10cm H 2O at rest and increased to values as high as −160 cm H 2O during the vibration response. Suction intensity increased in direct proportion to the amplitude of the vibratory stimulus. Most of the suction response was lost following labyrinthectomy. Electromyographic recordings from the pharyngeal dilator m. basilaris and the lingual retractor m. cardioapicalis revealed stimulus-locked activity which preceded increased suction in adults, however, no vibration-evoked electromyogram responses were noted while recording from the gill chamber musculature or funnel. Stimulus-locked efferent activity was observed in the V-basilaris and V-apicalis branches of both trigeminal nerves following vibration of an otic capsule. Efferent vibration-evoked activity was lost in the trigeminal nerve after labyrinthectomy. No vibration-evoked activity was observed in nerves IX or X. Sudden vibration evoked dramatically different responses in larval and adult lampreys. Larvae contracted their gill chambers and expelled water from their mouths while adults exhibited a powerful suction reflex and no gill contraction. The trigeminal components of these behaviors (including velum and oral hood movement in larvae, pharynx and apicalis movement in adults) are difficult to compare. All of the larval trigeminal muscles degenerate during metamorphosis and are replaced by new adult muscles [ M. W. Hardisty and C. M. Rovainen (1982) In The Biology of Lampreys, Vol. 4A. Academic Press, London]. The major muscles of the gill chamber, however, are spared during metamorphosis. Gill musculature is innervated by cranial nerves IX and X. We observed a vibration-evoked contraction of the gill chamber in larval lampreys, but not in adults. This result implies a central reorganization of some cranial reflex pathways during metamorphosis.