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Neuronal Basis of Hunting and Feeding Behaviour in the Pteropod Mollusc Clione Limacina

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Neuronal Basis of Hunting and Feeding Behaviour in the Pteropod Mollusc Clione Limacina NEURONAL BASIS OF HUNTING AND FEEDING BEHAVIOUR IN THE PTEROPOD MOLLUSC CLIONE LIMACINA by Y. V. PANCHIN1,2,4, G. N. GAMKRELIDZE4, L. B. POPOVA4, T. G. DELIAGINA3,4, G. N. ORLOVSKY3,4 and Y. I. ARSHAVSKY1,2 (1Institute of Problemsof InformationTransmission, Academy of Sciencesof Russia;2 Departmentof Biology,University of California,San Diego,La Jolla, CA 92093, USA; 3 Nobel Institutefor Neurophysiology,Department ofNeuroscience, Karolinska Institutel, 17177 Stockholm,Sweden; 4 A. N. BelozerskyInstitute of Physico-ChemicalBiology, Moscow State University,Russia) ABSTRACT The pteropod mollusc Clionelimacina is a predator, feeding on another pteropod mol- lusc, Limacinahelicina. Essential elements of Clione'shunting and feeding behaviour can be evoked pharmacologically. The sensory input driven by the presence of Limacinais mimicked by physostigmine (PhS), the acetylcholinesterase inhibitor. Injection of PhS into Clionebrought it to the state of hunting excitation accompanied by a reversal of the reaction to head stimulation. As a result, head stimulation, instead of a defence reac- tion, evoked active hunting behaviour. The 'fictive hunting behaviour', that is activa- tion of main motor systems participating in hunting behaviour, could be evoked in a preparation of the isolated central nervous system (CNS) by PhS application. To some extent, activation of the motor systems was realized through serotonergic mechanisms. GABAergic mechanisms also play an important role in the organization of Clione's feeding behaviour. GABA application to the preparation of the isolated CNS resulted in activation of the feeding rhythm generator and excitation of the motoneurons supplying the protractor tentacle muscles. The results show that in gastropod molluscs complex behaviour involving different functional systems may be described in terms of the activity of single identified neurons. KEYWORDS: mollusc, Clionelimacina, hunting behaviour, feeding behaviour, physostig- mine, GABA, serotonin. INTRODUCTION The main goal of neuroethological studies is to describe an animal's behaviour in terms of 'neuron-to-neuron interactions'. About fifteen years ago the pteropod mollusc Clione limacina was 'discovered' as a new object for neurocthological studies. An advantage of Clione for these studies is that, being one of the gastropod molluscs, it has rather complex behaviour. From the beginning of the 1980's neuronal net- works controlling the main functional systems in Clione have been studied (ARSHAVSKY et al., 1982, 1983, 1985, 1989, 1990, 1991 a,e, Correspondence to: Yuri I. Arshavsky, Department of Biology, 0357, University of Cali- fornia, San Diego, La Jolla, CA 92093, U.S.A. 171 1993a,b; HUANG & SATTERLIE, 1990; KABOTYANSKY & SAKHAROV, 1989; SATTERLIE, 1985, 1991, 1993; SATTERLIE & SPENCER, 1985). The data about organization of neuronal networks controlling different functions in Clione presented a good basis for studying its complex behaviour when different networks are involved in coordinated activ- ity. Clione is a predator, and one of the most complex forms of its behaviour is hunting and feeding behaviour. Clione feeds on another pteropod mollusc, Limacina helicina. The presence of Limacina in the water brings Clione to the state of hunting excitation. The most impor- tant manifestation of this state is a reversal of the reaction to head stimulation. Normally, head stimulation evokes a defence reaction, that is, an inhibition of wing oscillations and sinking (ARSHAVSKY etal., 1985, 1990, 1991a; SATTERLIE et al., 1985). In Clione excited by the presence of Limacina, the same stimulus evokes an active hunting reaction. This reaction is a complex synergy including an explosive extrusion of the tentacles, protraction of the radula, acceleration of locomotion and heart beat, changes in spatial orientation, etc. The goal of this work was to study what mechanisms organize co-operative activity of neural networks controlling different systems during Clione's hunting and feeding behaviour. Experiments were carried out at the White Sea Biological Station Kartesh. To study the neuronal basis of hunting behaviour it was necessary to evoke this behaviour in a reduced preparation. However, our primary attempts to evoke a hunting response by presenting Limacina to a semi- intact preparation produced no result. Even after slight damage, Clione stopped reacting to Limacina. The situation changed radically when it was found that Clione's hunting and feeding behaviour can be evoked pharmacologically by injection of some drugs into the mollusk. Two pharmacological substances were especially effective. They are phy- sostigmine (PhS), the acetylcholinesterase inhibitor, and GABA (ARSHA VSKY etal., 1991b-d, 1993a, b). PHYSOSTIGMINE Injection of PhS into the hemocoel, like the presence of Limacina, brought Clione into the state of hunting excitation. In Clione injected with PhS (- 1 0-6 M), a head stimulation evoked not the defence reac- tion, but the typical pattern of hunting behaviour with protraction of the tentacles, acceleration of locomotion, protraction of the radula, and changes of spatial orientation. PhS was found to be effective when applied to the isolated central nervous system (CNS). This presented a unique opportunity for studying the neuronal basis of Clione's hunting behaviour. .
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