Prey capture phase of feeding behavior in the pteropod mollusc, clione limacina: neuronal mechanisms

1995 ◽  
Vol 177 (1) ◽  
Author(s):  
T.P. Norekian
1996 ◽  
Vol 75 (2) ◽  
pp. 529-537 ◽  
Author(s):  
T. P. Norekian ◽  
R. A. Satterlie

1. The behavioral repertoire of the holoplanktonic pteropod mollusk Clione limacina includes a few well-defined behaviors organized in a priority sequence. Whole body withdrawal takes precedence over slow swimming behavior, whereas feeding behavior is dominant over withdrawal. In this study a group of neurons is described in the pleural ganglia, which controls whole body withdrawal behavior in Clione. Each pleural withdrawal (Pl-W) neuron has a high threshold for spike generation and is capable of inducing whole body withdrawal in a semi-intact preparation: retraction of the body-tail, wings, and head. Each Pl-W neuron projects axons into the main central nerves and innervates all major regions of the body. 2. Stimulation of Pl-W neurons produces inhibitory inputs to swim motor neurons that terminate swimming activity in the preparation. In turn, Pl-W neurons receive inhibitory inputs from the cerebral neurons involved in the control of feeding behavior in Clione, neurons underlying extrusion of specialized prey capture appendages. Thus it appears that specific inhibitory connections between motor centers can explain the dominance of withdrawal behavior over slow swimming and feeding over withdrawal in Clione.


2005 ◽  
Vol 93 (1) ◽  
pp. 305-315 ◽  
Author(s):  
Tigran P. Norekian ◽  
Aleksey Y. Malyshev

Coordination between different motor centers is essential for the orderly production of all complex behaviors. Understanding the mechanisms of such coordination during feeding behavior in the carnivorous mollusk Clione limacina is the main goal of the current study. A bilaterally symmetrical interneuron identified in the cerebral ganglia and designated Cr-BM neuron produced coordinated activation of neural networks controlling three main feeding structures: prey capture appendages called buccal cones, chitinous hooks used for prey extraction from the shell, and the toothed radula. The Cr-BM neuron produced strong excitatory inputs to motoneurons controlling buccal cone protraction. It also induced a prominent activation of the neural networks controlling radula and hook rhythmic movements. In addition to the overall activation, Cr-BM neuron synaptic inputs to individual motoneurons coordinated their activity in a phase-dependent manner. The Cr-BM neuron produced depolarizing inputs to the radula protractor and hook retractor motoneurons, which are active in one phase, and hyperpolarizing inputs to the radula retractor and hook protractor motoneurons, which are active in the opposite phase. The Cr-BM neuron used GABA as its neurotransmitter. It was found to be GABA-immunoreactive in the double-labeling experiments. Exogenous GABA mimicked the effects produced by Cr-BM neuron on the postsynaptic neurons. The GABA antagonists bicuculline and picrotoxin blocked Cr-BM neuron-induced PSPs. The prominent coordinating effect produced by the Cr-BM neuron on the neural networks controlling three major elements of the feeding behavior in Clione suggests that this interneuron is an important part of the higher-order system for the feeding behavior.


1995 ◽  
Vol 198 (9) ◽  
pp. 2025-2040 ◽  
Author(s):  
D Ritter ◽  
K Nishikawa

High-speed videography and muscle denervation experiments were used to quantify the feeding kinematics of Hemisus marmoratum and to test hypotheses of muscle function. The feeding behavior of H. marmoratum, which feeds on ants and termites, differs radically from that of other frogs that have been studied. During feeding in H. marmoratum, the tongue 'telescopes' straight out of the mouth, as opposed to the 'flipping' tongue trajectory observed in most other frogs. At the time of prey contact, two lateral lobes of tissue at the tongue tip envelop the prey. These lateral lobes are capable of applying significant pulling forces to the prey and the tongue is, therefore, described as prehensile. The trajectory of the tongue can be adjusted throughout protraction so that the frog can 'aim' its tongue in all three dimensions; distance, azimuth and elevation. Bilateral denervation of the genioglossus muscles results in a complete lack of tongue protraction, indicating that the genioglossus muscle is the main tongue protractor in H. marmoratum, as in other frogs. Thus, H. marmoratum provides strong evidence of functional conservatism of the genioglossus muscle within anurans. Bilateral denervation of the hyoglossus muscle indicates that although the hyoglossus is involved in several aspects of normal tongue retraction, including the prehensile capability of the tongue tip, it is not necessary for tongue retraction. Unilateral denervation of the genioglossus muscle causes significant deviation of the tongue towards the denervated side, providing evidence for a mechanism of lateral tongue aiming. On the basis of the kinematics of prey capture, the anatomy of the tongue and the results of the denervation experiments, we propose that H. marmoratum uses a hydraulic mechanism to protract its tongue.


1995 ◽  
Vol 73 (2) ◽  
pp. 353-366 ◽  
Author(s):  
John T. Beneski Jr. ◽  
John H. Larsen Jr. ◽  
Brian T. Miller

High-speed cinematography was used to investigate the prey-capture kinematics of six species of mole salamanders (Ambystomatidae). We compared the feeding behavior of the subgenus Ambystoma (A. californiense and A. macrodactylum) with that of the subgenus Linguaelapsus (A. mabeei, A. texanum, A. annulatum, and A. cingulatum). Prey capture by all six species is characterized by a 3-part gape cycle (a period of rapid mouth opening prior to extraoral tongue protraction, followed by a period of relatively stable gape angle during extraoral tongue protraction and retraction, followed by a period of rapid mouth closure), a tongue-extension cycle (protraction and retraction), and anterior head–body displacement. Among the six species, two distinct modes of prey capture are evident: (1) the Ambystoma mode (A. californiense, A. macrodactylum, A. mabeei, and A. texanum), and (2) the Linguaelapsus mode (A. annulatum and A. cingulatum). Most differences in prey-capture kinematics between the two modes are primarily differences of degree rather than the addition or loss of unique behaviors, and include a general reduction in the gape angles and a general increase in the elapsed times associated with specific events in the Linguaelapsus mode. We hypothesize that these differences are primarily the result of a prolonged period of tongue protraction in the Linguaelapsus mode during which the glandular tongue pad is fitted to the prey. In addition to differing from each other, the gape profiles of the ambystomatid subgenera differ markedly from the 4-part gape profiles of plethodontids and salamandrids.


1993 ◽  
Vol 69 (2) ◽  
pp. 512-521 ◽  
Author(s):  
Y. I. Arshavsky ◽  
T. G. Deliagina ◽  
G. N. Gamkrelidze ◽  
G. N. Orlovsky ◽  
Y. V. Panchin ◽  
...  

1. The pteropod mollusk Clione limacina is a predator, feeding on the small pteropod mollusk Limacina helicina. Injection of gamma-aminobutyric acid (GABA) into the hemocoel of the intact Clione evoked some essential elements of the hunting and feeding behavior, i.e., protracting the tentacles, opening the mouth, and triggering the rhythmic movements of the buccal mass. This pattern resembled that evoked by presentation of the prey: Clione grasped the Limacina by its tentacles, extracted the prey's body from the shell and then swallowed it. 2. In electrophysiological experiments, several targets of GABA action have been found: 1) direct application of GABA to isolated cerebral motor neurons projecting to the protractor muscles of tentacles resulted in their excitation; 2) GABA activated the feeding rhythm generator located in the buccal ganglia; 3) GABA exerted excitatory or inhibitory effects on the receptor cells of statocysts, the effects being mediated by the efferent input to these cells; 4) GABA suppressed the defense reaction, which is an inhibition of the locomotor activity and of tentacle motor neurons, arising in response to stimulation of the head afferents; and 5) GABA potentiated an excitatory action of the serotoninergic metacerebral cells on the feeding rhythm generator. 3. Effects of GABA on the tentacle motor neurons and the feeding rhythm generator are pharmacologically distinguishable. The action of GABA on the feeding rhythm generator was mimicked by baclofen (which activates the GABAB receptors in mammalian neurons) and was not sensitive to bicuculline (the GABAA receptor antagonist in mammals). On the other hand, bicuculline competitively inhibited the GABA-induced excitation of the tentacle motor neurons. 4. GABAergic neurons have been located in the cerebral, pedal, and buccal ganglia by means of immunohistochemical methods.


1992 ◽  
Vol 182 (1) ◽  
pp. 1-7 ◽  
Author(s):  
C. O. Hermans ◽  
R. A. Satterlie

2013 ◽  
Vol 91 (6) ◽  
pp. 405-412 ◽  
Author(s):  
E. Ito ◽  
S. Kojima ◽  
K. Lukowiak ◽  
M. Sakakibara

The neural circuitry comprising the central pattern generator (CPG) that drives feeding behavior in the great pond snail (Lymnaea stagnalis (L., 1758)) has been worked out. Because the feeding behavior undergoes associative learning and long-term memory (LTM) formation, it provides an excellent opportunity to study the causal neuronal mechanisms of these two processes. In this review, we explore some of the possible causal neuronal mechanisms of associative learning of conditioned taste aversion (CTA) and its subsequent consolidation processes into LTM in L. stagnalis. In the CTA training procedure, a sucrose solution, which evokes a feeding response, is used as the conditioned stimulus (CS) and a potassium chloride solution, which causes a withdrawal response, is used as the unconditioned stimulus (US). The pairing of the CS–US alters both the feeding response of the snail and the function of a pair of higher order interneurons in the cerebral ganglia. Following the acquisition of CTA, the polysynaptic inhibitory synaptic input from the higher order interneurons onto the feeding CPG neurons is enhanced, resulting in suppression of the feeding response. These changes in synaptic efficacy are thought to constitute a “memory trace” for CTA in L. stagnalis.


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