Pharmacologically induced elements of the hunting and feeding behavior in the pteropod mollusk Clione limacina. I. Effects of GABA

1993 ◽  
Vol 69 (2) ◽  
pp. 512-521 ◽  
Author(s):  
Y. I. Arshavsky ◽  
T. G. Deliagina ◽  
G. N. Gamkrelidze ◽  
G. N. Orlovsky ◽  
Y. V. Panchin ◽  
...  
Keyword(s):  
Feeding Behavior ◽  
Motor Neurons ◽  
Gabab Receptors ◽  
Gamma Aminobutyric Acid ◽  
Rhythmic Movements ◽  
Rhythm Generator ◽  
Buccal Ganglia ◽  
Gabaa Receptor Antagonist ◽  
Feeding Rhythm ◽  
Clione Limacina

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.

Whole body withdrawal circuit and its involvement in the behavioral hierarchy of the mollusk Clione limacina

1996 ◽  
Vol 75 (2) ◽  
pp. 529-537 ◽  
Author(s):  
T. P. Norekian ◽  
R. A. Satterlie
Keyword(s):  
Feeding Behavior ◽  
Motor Neurons ◽  
Prey Capture ◽  
The Body ◽  
Whole Body ◽  
High Threshold ◽  
Behavioral Repertoire ◽  
Withdrawal Behavior ◽  
Cerebral Neurons ◽  
Clione Limacina

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.

scholarly journals Phase-Locked Coordination Between Two Rhythmically Active Feeding Structures in the Mollusk Clione limacina. I. Motor Neurons

2002 ◽  
Vol 87 (6) ◽  
pp. 2996-3005 ◽  
Author(s):  
Aleksey Y. Malyshev ◽  
Tigran P. Norekian
Keyword(s):  
Central Pattern Generator ◽  
Motor Neurons ◽  
Electrical Coupling ◽  
Pattern Generator ◽  
Dependent Manner ◽  
Synaptic Connections ◽  
Buccal Ganglia ◽  
Active Feeding ◽  
Clione Limacina ◽  
Specific Phase

Coordination between different motor centers is essential for the orderly production of all complex behaviors, in both vertebrates and invertebrates. The current study revealed that rhythmic activities of two feeding structures of the pteropod mollusk Clione limacina, radula and hooks, which are used to extract the prey from its shell, are highly coordinated in a phase-dependent manner. Hook protraction always coincided with radula retraction, while hook retraction coincided with radula protraction. Thus hooks and radula were always moving in the opposite phases, taking turns grabbing and pulling the prey tissue out of the shell. Identified buccal ganglia motor neurons controlling radula and hooks protraction and retraction were rhythmically active in the same phase-dependent manner. Hook protractor motor neurons were active in the same phase with radula retractor motor neurons, while hook retractor motor neurons burst in phase with radula protractor motor neurons. One of the main mechanisms underlying the phase-locked coordination was electrical coupling between hook protractor and radula retractor motor neurons. In addition, reciprocal inhibitory synaptic connections were found between hook protractor and radula protractor motor neurons. These electrical and inhibitory synaptic connections ensure that rhythmically active hooks and radula controlling motor neurons are coordinated in the specific phase-dependent manner described above. The possible existence of a single multifunctional central pattern generator for both radula and hook motor centers is discussed.

Inhibitory transmission in the basolateral amygdala

1991 ◽  
Vol 66 (3) ◽  
pp. 999-1009 ◽  
Author(s):  
D. G. Rainnie ◽  
E. K. Asprodini ◽  
P. Shinnick-Gallagher
Keyword(s):  
Reversal Potential ◽  
Nmda Antagonist ◽  
Gabab Receptors ◽  
Excitatory Postsynaptic Potential ◽  
Sodium Pentobarbital ◽  
Gamma Aminobutyric Acid ◽  
Gabaa Receptor Antagonist ◽  
Basolateral Nucleus ◽  
Stimulation Of ◽  
Synaptic Responses

1. Intracellular recording techniques were used to characterize synaptic inhibitory postsynaptic potentials (IPSPs) recorded from neurons of the basolateral nucleus of the amygdala (BLA). Bipolar electrodes positioned in the stria terminalis (ST) or lateral amygdala (LA) were used to evoke synaptic responses at a frequency of 0.25 Hz. 2. Two synaptic waveforms having IPSP components could be evoked by electrical stimulation of either pathway: a biphasic, excitatory postsynaptic potential (EPSP), fast-IPSP (f-IPSP) waveform, and a multiphasic, EPSP, f-IPSP, and subsequent slow-IPSP (s-IPSP) waveform. Expression of either waveform was dependent on the site of stimulation. ST stimulation evoked a similar number of biphasic (45%) and multiphasic (50%) synaptic responses. In contrast, stimulation of the LA pathway evoked mainly (80%) multiphasic synaptic responses. 3. Both the f- and s-IPSP elicited by ST stimulation could be reduced in amplitude in the presence of the glutamatergic, N-methyl-D-aspartate (NMDA) antagonist, (DL)-2-amino-5-phosphonovaleric acid (APV, 50 microM), and were abolished by the glutamatergic, non-NMDA antagonist, 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX, 10 microM). In contrast, a CNQX-resistant f-IPSP was evoked with LA stimulation and abolished by subsequent addition of bicuculline methiodide (BMI), a gamma-aminobutyric acid (GABAA) receptor antagonist, suggesting direct inhibition of BLA neurons by GABAergic LA interneurons. The sensitivity of the s-IPSPs and the f-IPSPs to glutamatergic antagonists suggests the presence of feed-forward inhibition onto BLA neurons. 4. The f-IPSP possessed characteristics of potentials mediated by GABAA receptors linked to Cl- channels, namely, a reversal potential of -70 mV, a decrease in membrane resistance (13.5 M omega) recorded at -60 mV, a block by BMI, and potentiation by sodium pentobarbital (NaPB). 5. The s-IPSP was associated with a resistance decrease of 4.5 M omega, a reversal potential of -95 mV, and was reversibly depressed (approximately 66%) by 2-hydroxy-saclofen (100 microM), suggesting activation of GABAB receptors. 6. The large resistance change associated with the f-IPSP, its temporal overlap with evoked EPSPs, and the development of both spontaneous and evoked burst firing in the presence of BMI suggests that the f-IPSP determines the primary state of excitability in BLA neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Esophageal mechanoreceptors in the feeding system of the pond snail, Lymnaea stagnalis

1989 ◽  
Vol 61 (4) ◽  
pp. 727-736 ◽  
Author(s):  
C. J. Elliott ◽  
P. R. Benjamin
Keyword(s):  
Feeding Behavior ◽  
Synaptic Input ◽  
Lymnaea Stagnalis ◽  
Esophageal Wall ◽  
Pond Snail ◽  
Feeding System ◽  
Buccal Ganglia ◽  
Feeding Rhythm ◽  
Feeding Cycle ◽  
Stimulation Of

1. We identify esophageal mechanoreceptor (OM) neurons of Lymnaea with cell bodies in the buccal ganglia and axons that branch repeatedly to terminate in the esophageal wall. 2. The OM cells respond phasically to gut distension. Experiments with a high magnesium/low calcium solution suggest that the OM neurons are primary mechanoreceptors. 3. In the isolated CNS preparation, the OM cells receive little synaptic input during the feeding cycle. 4. The OM cells excite the motoneurons active in the rasp phase of the feeding cycle. 5. The OM cells inhibit each of the identified pattern-generating and modulatory interneurons in the buccal ganglia. Experiments with a saline rich in magnesium and calcium suggest that the connections are monosynaptic. 6. Stimulation of a single OM cell to fire at 5-15 Hz is sufficient to terminate the feeding rhythm in the isolated CNS preparation. 7. We conclude that these neurons play a role in terminating feeding behavior.

Inhibition of transmitter release shortens the duration of the excitatory synaptic current at a calyceal synapse

1996 ◽  
Vol 76 (5) ◽  
pp. 3584-3588 ◽  
Author(s):  
T. S. Otis ◽  
L. O. Trussell
Keyword(s):  
Transmitter Release ◽  
Time Course ◽  
Receptor Activation ◽  
Gabab Receptors ◽  
Aminobutyric Acid ◽  
Gamma Aminobutyric Acid ◽  
Synaptic Currents ◽  
Quantal Release ◽  
Epsc Amplitude ◽  
Gabaa Receptor Antagonist

1. We investigated the effect of reducing transmitter release on the time course of multiquantal, evoked synaptic currents to test for transmitter “cross talk” between neighboring synaptic release sites within a calyceal synapse. By using a brain slice preparation, neurons in the chick nucleus magnocellularis (nMAG) were voltage clamped and individual presynaptic axons were stimulated to evoke excitatory postsynaptic currents (EPSCs). 2. Application of 100-microM baclofen or 50-microM GABA in the presence of a gamma-aminobutyric acid-A (GABAA) receptor antagonist produced an 85% reduction of EPSCs, consistent with the activation of presynaptic gamma-aminobutyric acid-B (GABAB) receptors. In parallel with the reduction in the amplitude of the EPSC by GABAB receptor activation, the normally strong paired pulse depression (PPD) of the EPSC was converted to facilitation. The reduction in EPSC amplitude by gamma-aminobutyric acid (GABA) or baclofen was accompanied by a 20% reduction in the exponential time constant of decay of the EPSC. Weaker effects on the EPSC time course were observed for synapses with the least PPD. 3. Cd2+ (5 microM), which inhibits presynaptic calcium current, also reduced EPSC amplitude by 85% and converted PPD to facilitation. EPSCs were narrower in Cd2+, though less so than in baclofen. 4. The time course of the EPSC was longer than that of miniature synaptic currents, even after significant block by baclofen, GABA or Cd2+, indicating that dispersion of quantal release may help shape the synaptic waveform. However, the narrowing of the EPSC by baclofen, GABA, and Cd2+ suggests that high levels of quantal release at the calyceal synapse may delay the removal of transmitter, further slowing the EPSC.

Enteric GABA: mode of action and role in the regulation of the peristaltic reflex

1992 ◽  
Vol 262 (4) ◽  
pp. G690-G694 ◽  
Author(s):  
J. R. Grider ◽  
G. M. Makhlouf
Keyword(s):  
Receptor Antagonist ◽  
Motor Neurons ◽  
Gabaa Receptors ◽  
Mode Of Action ◽  
Gabab Receptor ◽  
Circular Muscle ◽  
Gamma Aminobutyric Acid ◽  
Peristaltic Reflex ◽  
Gaba Neurons ◽  
Gabaa Receptor Antagonist

The mode of action of gamma-aminobutyric acid (GABA) and the role of myenteric GABA neurons in the regulation of peristalsis were examined in various preparations of rat colonic muscle. GABA had no contractile, relaxant, or modulatory effect on smooth muscle cells isolated from the circular muscle layer. In innervated circular muscle strips, GABA elicited concentration-dependent relaxation accompanied by release of vasoactive intestinal peptide (VIP). Relaxation and VIP release were inhibited by tetrodotoxin and by the GABAA receptor antagonist bicuculline but not by the GABAB receptor antagonist phaclofen. Relaxation was inhibited by the VIP receptor antagonist VIP-(10-28) implying that VIP release was coupled to muscle relaxation. Relaxation was augmented by atropine implying that GABA also activated cholinergic neurons causing release of acetylcholine that attenuated the relaxant response. This pharmacological profile was evident when GABA was released from intrinsic GABA neurons during peristalsis induced by radial stretch. Blockade of GABAA receptors with bicuculline inhibited the descending relaxation mediated by VIP motor neurons and the ascending contraction mediated by cholinergic motor neurons. Stimulation of these receptors with exogenous GABA had the opposite effect. We conclude that on release from myenteric neurons, GABA acts via GABAA receptors on cholinergic and VIP motor neurons responsible for the two components of the peristaltic reflex.

Activity patterns of the B31/B32 pattern initiators innervating the I2 muscle of the buccal mass during normal feeding movements in Aplysia californica

1996 ◽  
Vol 75 (4) ◽  
pp. 1309-1326 ◽  
Author(s):  
I. Hurwitz ◽  
D. Neustadter ◽  
D. W. Morton ◽  
H. J. Chiel ◽  
A. J. Susswein
Keyword(s):  
Feeding Behavior ◽  
Motor Neurons ◽  
Activity Patterns ◽  
Aplysia Californica ◽  
Motor Programs ◽  
Physiological Functions ◽  
Rest Position ◽  
Buccal Ganglia ◽  
Normal Feeding ◽  
Protraction Phase

1. B31 and B32 are pattern-initiator neurons in the buccal ganglia of Aplysia. Along with the B61/B62 neurons, B31/B32 are also motor neurons that innervate the 12 buccal muscle via the I2 nerve. This research was aimed at determining the physiological functions of the B31/B32 and B61/B62 neurons, and of the I2 muscle. 2. Stimulating the I2 muscle in the radula rest position produces radula protraction. In addition, in behaving animals lesioning either the muscle or the I2 nerve greatly reduces radula protraction. 3. During buccal motor programs in reduced preparations, B31/B32 and B61/62 fire preceding activity in neuron B4, whose firing indicates the onset of radula retraction. In addition, during both ingestion-like and rejection-like patterns the activity in the I2 nerve is correlated with protraction. 4. B31/B32 fire at frequencies of 15-25 Hz. Neither B31/B32 nor B61/B62 elicit facilitating end-junction potentials (EJPs) and electromyograms (EMGs) in the I2 muscle. EMGs from B31/B32 are smaller than those from B61/B62. B31/B32 and B61/B62 innervate all areas of the muscle approximately uniformly. 5. In behaving animals, EMGs consistent with B31/B32 activity are seen in the I2 muscle during the protraction phase of biting, swallowing, and rejection movements. In addition, the I2 muscle receives inputs that cannot be attributed to either the B31/B32 or B61/B62 neurons, either because the potentials are too large, firing frequencies are too low, or a prominent facilitation is seen. Such potentials are associated with lip movements, and also with radula retraction. 6. EMGs were recorded from the I2 muscle during feeding behavior after a lesion of the I2 nerve. Animals that had severe deficits in protraction showed no activity consistent with B31/B32 or B61/B62, but did show activity during retraction. 7. Our data indicate that the I2 muscle and the B31/B32 motor neurons are essential constituents contributing to protraction movements. Activity in these neurons is associated with radula protraction, which occurs as a component of a number of different feeding movements. The I2 muscle may also contribute to retraction, via activation by other motor neurons.

Coordinated Excitatory Effect of GABAergic Interneurons on Three Feeding Motor Programs in the Mollusk Clione limacina

2005 ◽  
Vol 93 (1) ◽  
pp. 305-315 ◽  
Author(s):  
Tigran P. Norekian ◽  
Aleksey Y. Malyshev
Keyword(s):  
Neural Networks ◽  
Feeding Behavior ◽  
Prey Capture ◽  
Order System ◽  
Dependent Manner ◽  
Rhythmic Movements ◽  
Excitatory Effect ◽  
Double Labeling ◽  
The Neural Networks ◽  
Clione Limacina

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.

Control of feeding motor output by paracerebral neurons in brain of Pleurobranchaea californica

1982 ◽  
Vol 47 (5) ◽  
pp. 885-908 ◽  
Author(s):  
R. Gillette ◽  
M. P. Kovac ◽  
W. J. Davis
Keyword(s):  
Feeding Behavior ◽  
Action Potentials ◽  
Tactile Stimulation ◽  
Natural Food ◽  
Buccal Ganglion ◽  
Pleurobranchaea Californica ◽  
Feeding Rhythm ◽  
Intracellular Stimulation ◽  
Motor Rhythm ◽  
Stimulation Of

1. A population of interneurons that control feeding behavior in the mollusk Pleurobranchaea has been analyzed by dye injection and intracellular stimulation/recording in whole animals and reduced preparations. The population consists of 12-16 somata distributed in two bilaterally symmetrical groups on the anterior edge of the cerebropleural ganglion (brain). On the basis of their position adjacent to the cerebral lobes, these cells have been named paracerebral neurons (PCNs). This study concerns pme subset pf [MCs. the large, phasic ones, which have the strongest effect on the feeding rhythm (21). 2. Each PCN sends a descending axon via the ipsilateral cerebrobuccal connective to the buccal ganglion. Axon branches have not been detected in other brain or buccal nerves and hence the PCNs appear to be interneurons. 3. In whole-animal preparations, tonic intracellular depolarization of the PNCs causes them to discharge cyclic bursts of action potentials interrupted by a characteristic hyperpolarization. In all specimens that exhibit feeding behavior, the interburst hyperpolarization is invariably accompanied by radula closure and the beginning of proboscis retraction (the "bite"). No other behavorial effect of PCN stimulation has been observed. 4. In whole-animal preparations, the PCNs are excited by food and tactile stimulation of the oral veil, rhinophores, and tentacles. When such stimuli induce feeding the PCNs discharge in the same bursting pattern seen during tonic PCN depolarization, with the cyclic interburst hyperpolarization phase locked to the bit. When specimens egest an unpalatable object by cyclic buccal movements, however, the PCNs are silent. The PCNs therefore exhibit properties expected of behaviorally specific "command" neurons for feeding. 5. Silencing one or two PCNs by hyperpolarization may weaken but does not prevent feeding induced by natural food stimuli. Single PCNs therefore can be sufficient but are not necessary to induction of feeding behavior. Instead the PCNs presumably operate as a population to control feeding. 6. In isolated nervous system preparations tonic extracellular stimulation of the stomatogastric nerve of the buccal ganglion elicits a cyclic motor rhythm that is similar in general features to the PNC-induced motor rhythm. Bursts of PCN action potentials intercalated at the normal phase position in this cycle intensify the buccal rhythm. Bursts of PCN impulses intercalated at abnormal phase positions reset the buccal rhythm. The PCNs, therefore, also exhibit properties expected of pattern-generator elements and/or coordinating neurons for the buccal rhythm. 7. The PCNs are recruited into activity when the buccal motor rhythm is elicited by stomatogastric nerve stimulation or stimulation of the reidentifiable ventral white cell. The functional synergy between the PCNs and the buccal rhythm is therefore reciprocal. 8...

Differential firing patterns of the peptide-containing cholinergic motor neurons B15 and B16 during feeding behavior inAplysia

1990 ◽  
Vol 522 (1) ◽  
pp. 176-179 ◽  
Author(s):  
Elizabeth C. Cropper ◽  
Irving Kupfermann ◽  
Klaudiusz R. Weiss
Keyword(s):  
Feeding Behavior ◽  
Motor Neurons ◽  
Firing Patterns
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