An identified cerebral interneuron initiates different elements of prey capture behavior in the pteropod mollusc,Clione limacina

The prey capture phase of feeding behavior in the pteropod molluscClione limacina consists of an explosive extrusion of buccal cones, specialized oral appendages which are used to catch the prey, and significant acceleration of swimming. Several groups of neurons which control different components of prey capture behavior inClione have been previously identified in the CNS. However, the question of their coordination in order to develop a normal behavioral reaction still remains open. We describe here a cerebral interneuron which has wide-spread excitatory and inhibitory effects on a number of neurons in the cerebral and pedal ganglia, directed toward the initiation of prey capture behavior inClione. This bilaterally symmetrical neuron, designated Cr-PC (Cerebral interneuron initiating Prey Capture), produced monosynaptic activation of Cr-A motoneurons, which control buccal cone extrusion, and inhibition of Cr-B and Cr-L motoneurons, whose spike activities maintain buccal cones in a withdrawn position inside the head in non-feeding animals. In addition, Cr-PC produced monosynaptic activation of a number of swim motoneurons and interneurons of the swim central pattern generator (CPG) in the pedal ganglia, pedal serotonergic Pd-SW neurons involved in a peripheral modulation of swimming and the serotonergic Heart Excitor neuron.     

Mechanisms of Locomotory Speed Change: The Pteropod Solution

Three primary factors contribute to locomotory speed changesin the pteropod mollusk Clione limacina. (1) An increase incycle frequency of locomotory appendages is associated witha baseline depolarization and enhancement of postinhibitoryrebound in central pattern generator (CPG) interneurons, anda reorganization of the CPG through recruitment of additionalinterneurons. (2) An increase in the force of appendage movementsis generated through enhancement of activity of active motoneurons,recruitment of additional motoneurons and peripheral modulationof swim musculature. (3) Changes in biomechanical aspects ofappendage movements are presumably achieved, at least in part,through changes in the activity of motoneurons and swim muscle.All changes associated with non-startle swim acceleration areproduced by a serotonergic arousal system that acts at all threelevels of the swimming system: CPG interneurons, motoneuronsand swim musculature.     

Homologues of serotonergic central pattern generator neurons in related nudibranch molluscs with divergent behaviors

Homologues of a neuron that contributes to a species-specific behavior were identified and characterized in species lacking that behavior. The nudibranch Tritonia diomedea swims by flexing its body dorsally and ventrally. The dorsal swim interneurons (DSIs) are components of the central pattern generator (CPG) underlying this rhythmic motor pattern and also activate crawling. Homologues of the DSIs were identified in six nudibranchs that do not exhibit dorsal–ventral swimming: Tochuina tetraquetra, Melibe leonina, Dendronotus iris, D. frondosus, Armina californica, and Triopha catalinae. Homology was based upon shared features that distinguish the DSIs from all other neurons: (1) serotonin immunoreactivity, (2) location in the Cerebral serotonergic posterior (CeSP) cluster, and (3) axon projection to the contralateral pedal ganglion. The DSI homologues, named CeSP-A neurons, share additional features with the DSIs: irregular basal firing, synchronous inputs, electrical coupling, and reciprocal inhibition. Unlike the DSIs, the CeSP-A neurons were not rhythmically active in response to nerve stimulation. The CeSP-A neurons in Tochuina and Triopha also excited homologues of the Tritonia Pd5 neuron, a crawling efferent. Thus, the CeSP-A neurons and the DSIs may be part of a conserved network related to crawling that may have been co-opted into a rhythmic swim CPG in Tritonia. This material is based upon work supported by the National Science Foundation, under Grant No. 0445768, and a GSU Research Program Enhancement grant to PSK.     

Differential effects of serotonergic and peptidergic cardioexcitatory neurons on the heart activity in the pteropod mollusc, Clione limacina

A group of four cardioexcitatory neurons has been identified in the intestinal ganglia of the mollusc Clione limacina. Relatively weak stimulation of the intestinal neurons induced auricle contractions only, while strong stimulation produced initial auricle contractions followed by full-cycle auricle-ventricle contractions. Intestinal cardioexcitatory neurons probably utilized as their transmitter a peptide similar to Tritonia pedal peptide – they showed pedal peptide-like immunoreactivity, and their effects were mimicked by application of the exogenous pedal peptide. The pedal cardioexcitatory neuron was found to produce strong excitatory effects only on the ventricle contractions. Its stimulation induced ventricle contractions in the quiescent heart or significantly accelerated the rate of ventricle contractions in the rhythmically active heart. The pedal cardioexcitatory neuron apparently utilized serotonin as a neurotransmitter, based upon serotonin immunoreactivity, blocking effect of serotonin antagonists mianserin and methysergide, and the observation that exogenous serotonin mimicked its effect. A dense network of pedal peptide-like immunoreactivity was found both in the auricle and ventricle tissue. Serotonin immunoreactivity was densely present in the ventricle, while the auricle contained only a separate serotonin-immunoreactive unbranched axon. Thus, there are two separate groups of central cardioexcitatory neurons with different effects on heart activity, which together might provide a complex cardio-regulatory function in Clione. Accepted: 14 August 1999     

Serotonergic Neural System not only Activates Swimming but also Inhibits Competing Neural Centers in a Pteropod Mollusc

Initiation of a particular behavior requires not only activationof the neural center directly involved in its control but alsoinhibition of the neural networks controlling competing behaviors.In the pteropod mollusc, Clione limacina, many identified serotonergicneurons activate or modulate different elements of the swimmingsystem resulting in the initiation or acceleration of the swimmingbehavior. Cerebral serotonergic neurons are described here,which produce excitatory inputs to the swimming system as wellas inhibitory inputs to the neural centers that control competingbehaviors. Whole-body withdrawal behavior is incompatible withswimming activity in Clione. The main characteristic of whole-bodywithdrawal is complete inhibition of swimming. Cerebral serotonergicneurons were found to produce a prominent inhibition of thepleural neurons that control whole-body withdrawal behavior.By inhibiting pleural withdrawal cells, serotonergic neuronseliminate its inhibitory influence on the swimming system andthus favor increased swimming speed. Serotonergic neurons alsoproduce a prominent inhibition of the Pleural White Cell, whichis presumably involved in reproductive or egg-laying behavior.Thus the serotonergic system directly activates swimming systemand, at the same time, alters a variety of other neural systemspreventing simultaneous initiation of incompatible behaviors.     

The role of postinhibitory rebound in the locomotor central-pattern generator of Clione limacina

In animals, networks of central neurons, called central-patterngenerators (CPGs), produce a variety of locomotory behaviorsincluding walking, swimming, and flying. CPGs from diverse animalsshare many common characteristics that function at the systemlevel, circuit level, and cellular level. However, the relativeroles of common CPG characteristics are variable among differentanimal species, in ways that suit different forms of locomotionin different environmental contexts. Here, we examine some ofthese common features within the locomotor CPG in a model systemused to investigate changes in locomotory speed—the swimsystem of the pteropod mollusk, Clione limacina. In particular,we discuss the role of one cellular characteristic that is essentialfor locomotor pattern generation in Clione, postinhibitory rebound.     

Pedal serotonergic neurons modulate the synaptic input of withdrawal interneurons ofHelix

A group of serotonergic cells, located in the pedal ganglia ofHelix lucorum, modulates synaptic responses of neurons involved in withdrawal behavior. Extracellular or intracellular stimulation of these serotonergic cells leads to facilitation of spike responses to noxious stimuli in the putative command neurons for withdrawal behavior. Noxious tactile stimuli elicit an increase in background spiking frequency in the modulatory neurons and a corresponding increase in stimulus-evoked spike responses in withdrawal interneurons. The serotonergic neurons have processes in the neuropil of the parieto-visceral ganglia complex, consistent with their putative role in modulating the activity of giant parietal interneurons, which send processes to the same neuropil and to the pedal ganglia. The serotonergic cells respond to noxious tactile and chemical stimuli. Although the group as a whole respond to noxious stimuli applied to any part of the body, most cells respond more to ipsilateral than contralateral stimulation, and exhibit differences in receptive areas. Intracellular investigation revealed electrical coupling between serotonergic neurons which could underlie the recruitment of members of the group not responding to a given noxious stimulus.     

Neural control of heartbeat in the pteropod mollusk Clione limacina

The heart of the pteropod molluskClione limacina is innervated by the median nerve arising from the left abdominal ganglion. Five neurons sending axons to the heart have been identified in theClione central nervous system with retrograde cobalt or Lucifer yellow staining. Neuron H1 located in the left pedal ganglion produced an excitatory effect on heart beat. Stimulation of three neurons, H2–H4, situated in a compact group in the medial region of the left abdominal ganglion, led to inhibition of cardiac contraction, while H5, located in the caudal region of the left abdominal ganglion, did not affect heart beat. The activity of efferent cardiac neurons (ECN) was found to be related to the operation of the locomotor rhythm generator. Spontaneous or reflex depression of the latter was found to inhibit neuron H1 and activate units H2–H4. The behavior of these ECN accounts for the positive correlation between heart operation and locomotor activity inClione limacina.Institute of Research on Information Transmission, Academy of Sciences of the USSR, Moscow, M. V. Lomonosov State University, Moscow. Translated from Neirofiziologiya, Vol. 21, No. 2, pp. 185–192, March–April, 1989.     

Neuronal control of pedal sole cilia in the pond snail Lymnaea stagnalis appressa

5-HT (serotonin) is a ubiquitous neurotransmitter that produces ciliary beating in gastropods when applied topically, but ciliary beating caused by gastropod serotonergic neurons has been described in only three neuron pairs. We extend these results to the North American Lymnaea stagnalis appressa, which is a different species from the European Lymnaea stagnalis. We describe a non-serotonergic neuron pair, PeV1, which accelerates pedal sole mucociliary transport and a serotonergic neuron pair, PeD7, which slows mucociliary transport. We compare and discuss development and identified neurons in L. s. appressa and in L. stagnalis, which have homologs to L. s. appressa PeD7 and PeV1 neurons. In addition to PeD7 and PeV1 neurons, we test neurons immunoreactive to Tritonia pedal peptide antibodies with negative results for mucociliary transport. In characterizing PeD7 and PeV1 neurons, we find that PeV1 does not excite PeD7. In semi-intact preparations, a strong increase in PeD7 neuron activity occurs during tactile stimulation, but V1 neurons are inhibited during tactile stimulation. Following tactile stimulation, PeV1 neurons show strong activity. This suggests a distinct difference in function of the two neuron pairs, which both have their axons overlying pedal sole ciliary cells. Application of 5-HT to the pedal sole initiates mucociliary transport in 1.4–1.9 s with a time course similar to that seen when stimulating a PeV1 neuron. This result appears to be through a 5-HT_1A-like receptor on the pedal sole. We describe a possible external source of 5-HT on the pedal sole from 5-HT immunoreactive granules that are released with mucus.     

Cerebral neurons underlying prey capture movements in the pteropod mollusc,Clione limacina

The pteropod mollusc Clione limacina is a highly specialized carnivore which feeds on shelled pteropods and uses, for their capture, three pairs of oral appendages, called buccal cones. Contact with the prey induces rapid eversion of buccal cones, which then become tentacle-like and grasp the shell of the prey. In the previous paper, a large group of electrically coupled, normally silent cells (A motoneurons) has been described in the cerebral ganglia of Clione. Activation of A neurons induces opening of oral skin folds and extrusion of the buccal cones. The present study continues the analysis of the electrical properties of A motoneurons.Brief intracellular stimulation of an A neuron can produce prolonged firing (afterdischarge), lasting up to 40 s, in the entire population of A neurons. Afterdischarge activity is based on an afterdepolarization evoked by an initial strong burst of A neuron spikes. The data suggest that this afterdepolarization represents excitatory synaptic input from unidentified neurons which in turn receive excitatory inputs from A neurons, thus organizing positive feedback. The main functional role of this positive feedback is the spread and synchronization of spike activity among all A neurons in the population. In addition, it serves to transform a brief excitatory input to A neurons into their prolonged and stable firing, which is required during certain phases of feeding behavior in Clione.