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1Arizona State University, School of Life Sciences, Tempe, Arizona; and 2Institute of Higher Nervous Activity and Neurophysiology, Moscow, Russia
Submitted 15 July 2004; accepted in final form 18 August 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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Clione is a highly specialized carnivore, which feeds only on two species of shelled pteropod mollusks of the genus Limacina (Lalli 1970
; Lalli and Gilmer 1989; Wagner 1885). To seize its prey, Clione rapidly protracts tentacle-like oral appendages, called buccal cones, which surround the Limacina shell and hold it during the subsequent phases of feeding. Once buccal cones have gripped the prey, they begin to manipulate it so that the shell aperture is pressed against the mouth of Clione. Then two other feeding structures, chitinous hooks and the radula, are used to extract the soft body of Limacina from its shell to be swallowed whole. The radula is a specialized structure found in all gastropod mollusks. Its rhythmic protraction-retraction movement is designed to seize the food and bring it to the opening of the esophagus. Chitinous hooks, which normally are retracted inside two symmetrical muscular hook sacs, are unique to Clione and other mollusks from the order Gymnosomata and reflect a high food specialization (Lalli 1970; Lalli and Gilmer 1989). The functional role of the hooks is to grab the soft body of Limacina and pull it out of the shell into the buccal cavity. Hook activity is also rhythmic and consists of protraction and retraction phases. We have shown in the previous investigation that the rhythmic movements of radula and hooks are highly coordinated in a phase-dependent manner (Malyshev and Norekian 2002). This phase-dependent coordination was observed on the behavioral level and was always recorded on the motoneuronal level during spontaneous and induced rhythmic activity. Hook protractor neurons were active in the same phase with radula retractor neurons, whereas hook retractor neurons were bursting in phase with radula protractor neurons (Malyshev and Norekian 2002).
We describe in this study and discuss the role of a bilaterally symmetrical cerebral interneuron, designated Cr-BM cell, which produces a prominent excitatory influence on all neural networks that control three major feeding structures in Clione: buccal cones, chitinous hooks, and the radula. A preliminary general description of some of these effects has been previously published (Norekian 1995). The overall strong excitatory influence produced by the Cr-BM neuron on all identified feeding neural networks is presumably important during the "prey extraction" period of the feeding behavior after the prey capture. In addition to the overall activation, the Cr-BM neuron has a strong coordinating influence on the individual elements of each neural network, which contributes to the phase-dependent coordination of their rhythmic activity. The Cr-BM interneuron apparently uses GABA as its excitatory transmitter based on double-labeling experiments, mimicking effect of exogenous GABA and blocking effects of GABA antagonists. This represents another interesting example of the excitatory role of GABA in the feeding behavior of Clione (Arshavsky et al. 1993; Norekian 1999).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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Intracellular recordings from individual neurons were made with glass microelectrodes (resistances: 10–30 M
) filled with 2 M potassium acetate. Electrophysiological signals were amplified, displayed, and recorded using conventional electrophysiological techniques. Intracellular stimulation was achieved via an amplifier bridge circuit. To test for monosynaptic connections, a high-divalent cation solution was used [containing (in mM) 110 MgCl2, 25 CaCl2, 400 NaCl, 10 KCl, and 3 NaHCO3, pH 7.4]. For morphological investigation of recorded neurons, a 5% solution of 5(6)-carboxyfluorescein (Sigma) prepared in 2 M potassium acetate was iontophoresed via the recording electrodes (resistances, 20–40 M) with 1- to 10-nA negative current pulses for 5–30 min. Injected cells were observed live in the recording dish with a Nikon epifluorescence microscope and with a BioRad (Hercules, CA) MRC 600 laser scanning confocal microscope.
GABA was applied locally to the soma of identified neurons via pressure ejection or iontophoretic application. For pressure ejection, glass micropipettes were filled with 5 mM GABA solution in filtered seawater and connected to the air-pressure system (PV830 Pneumatic PicoPump, WPI), which delivered pressure pulses of 40–60 p.s.i. and 200-ms duration. Fast Green dye (0.02%) was added in the solution for monitoring the drug delivery. For iontophoretic application, we used glass micropipettes with tip diameter 1–2 µm filled with 1 M GABA solution (pH 4). Iontophoretic currents had amplitude between 50 and 100 nA and were applied as brief pulses of 50- to 100-ms duration (Stimulator S4KR and Stimulus isolation unit SIU 4678, Grass instruments). GABA antagonists were applied with the use of a graduated 1-ml pipette. The final concentration was estimated from the known volume of injected solution and the known volume of saline in the recording dish.
For the whole-mount immunocytochemical procedure, the preparations were fixed for 3 h in 4% paraformaldehyde and 0.1% glutaraldehyde in PBS (pH = 6.5–7.0) at room temperature (15–20°C). To reduce high nonspecific fluorescence caused by glutaraldehyde fixation, the tissues were incubated overnight in 4% sodium borohydride in PBS (Kosaka et al. 1986). The preparations were washed for 12 h in PBS and preincubated in PBS containing 0.1% triton X-100 to increase tissue permeability. The tissues were then exposed to 6% goat serum in PBS and 0.1% Triton X-100 for 6 h to reduce nonspecific staining and incubated 36 h at 5°C in GABA antibody (polyclonal GABA antisera raised in guinea pig; Eugene Tech International, Ridgefield Park, NJ). The dilution of primary antibody was 1:500. After a 12-h wash in PBS, the tissues were placed for 24 h in fluorescein-labeled secondary antibody (working concentration 40 µg/ml; anti-guinea pig IgG produced in goat; Vector Labs, Burlingame, CA). The secondary antibody was removed with several PBS exchanges, and preparations were washed overnight. The tissues were then cleared in xylene, mounted in DPX, and examined in whole mount with a Nikon fluoresence microscope and a Bio-Rad MRC 600 laser scanning confocal microscope. The first set of control experiments included preadsorption of the primary antibody with 50 µM GABA-BSA conjugate for 6 h before processing the tissue. In the second set of controls, primary antibody was omitted from the procedure. No staining resulted in both sets of control experiments.
For double-labeling experiments, interneurons were injected with neurobiotin (Vector Laboratories). The preparations were then fixed in 4% paraphormaldehyde and 0.1% glutaraldehyde in PBS and incubated 12 h in Texas Red-labeled avidin (Vector Laboratories) to visualize neurobiotin-filled interneurons. The preparations were then processed for immunocytochemical reaction described in the preceding text. By switching filters in the fluorescence microscope or laser scanning confocal microscope for Texas Red and fluorescein, interneurons were identified as GABA-immunoreactive. Texas Red was not visible with the fluorescein filters, and fluorescein was not visible with the Texas Red filters, thus providing a clear comparison during filter switching.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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The bilaterally symmetrical Cr-BM interneuron was located on the ventral surface of the cerebral ganglia in the anterior region between the head nerves N1 and N2 that innervate the head of the animal (Fig. 1). The size of the cell body was 25–30 µm in diameter. A single large axon of the Cr-BM neuron exited the cerebral ganglia into the ipsilateral cerebro-buccal connective and innervated the neuropile of both buccal ganglia (Fig. 1). A few small processes also branched in the neuropile of the ipsilateral cerebral ganglion. The morphological structure of 16 Cr-BM interneurons was studied in 12 preparations after intracellular injection with the fluorescent dye carboxyfluorescein.
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). Radula retractor Bc-RR motoneurons were inhibited during this initial phase. In the hook controlling neural network, intracellular stimulation of the Cr-BM neuron produced initial burst of activity in the hook retractor Bc-HR motoneurons and inhibition of the hook protractor Bc-HP motoneurons, which were followed by a few cycles of rhythmic activity (n = 18; Fig. 2B). Stimulation of the Cr-BM interneurons also triggered a prominent spike activity in the Cr-A neurons, which control opening of the skin folds and buccal cone protraction (n = 32; Fig. 2C).
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The Cr-BM interneuron induced rhythmic activity in the buccal neural network controlling radula movements. Radula protractor motoneurons received prominent excitatory postsynaptic potentials (PSPs) from the Cr-BM neurons. Each induced Cr-BM neuron spike produced a single Bc-RP neuron excitatory PSP (EPSP), which persisted in the high-divalent solution, suggesting monosynaptic connection (n = 14; Fig. 3A). The Bc-PIN interneuron, which is active in the radula protraction phase, also received prominent excitatory inputs from the Cr-BM interneuron. Each Cr-BM spike generated a large-amplitude EPSP in the Bc-PIN cell, which persisted in high-divalent solution (n = 26; Fig. 3A). Radula retractor Bc-RR motoneurons received inhibitory inputs from the Cr-BM interneurons. Each induced Cr-BM neuron spike triggered a single Bc-RR neuron IPSP, which persisted in high-divalent solution, suggesting monosynaptic connection (n = 12; Fig. 3B). Thus having the overall excitatory effect on the radula controlling neural system, the Cr-BM neurons also produced coordinating inputs to the specific elements of this system ensuring that radula protractor and radula retractor neurons are active in the opposite phases of their rhythmic cycle.
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). The excitatory inputs from the Cr-BM neurons to the Cr-A neurons were highly efficient. However, they were apparently not monosynaptic; some of the induced Cr-BM neuron spikes failed in high-divalent solution to produce EPSPs in these cells (n = 17). In addition, in the reduced preparations that did not include buccal ganglia, the Cr-BM interneurons did not have any effect on the Cr-A neurons (n = 6). These experiments suggested that a polysynaptic connection between the Cr-BM interneurons and the Cr-A neurons occur via the buccal ganglia. To confirm this suggestion, the following experiments were performed. In the semi-intact preparations, several prominent excitatory inputs in the Cr-A neurons triggered by induced bursts of spikes in the Cr-BM interneurons were recorded. Then the ipsilateral cerebro-buccal connective was cut with fine scissors. After the cut, all Cr-BM neuron-induced responses in the Cr-A neurons completely disappeared (n = 5; Fig. 5A). One of the buccal interneurons, which could be involved in the transition of the excitatory inputs from the Cr-BM interneuron to the Cr-A neurons, was Bc-PIN interneuron. The Bc-PIN interneuron has been previously shown to send an individual axon to the cerebral ganglia and produce activation of the Cr-A neurons ("tentacle motoneurons" according to Arshavsky et al. 1993). We have found that these excitatory inputs from the Bc-PIN neuron to the Cr-A neurons were apparently monosynaptic. Each induced Bc-PIN neuron spike produced an individual EPSP in the Cr-A neurons, which persisted without failure in high-divalent solution (n = 11; Fig. 5B). Simultaneous recordings from the Cr-BM, Bc-PIN, and the Cr-A neurons revealed that the Bc-PIN neuron was always spiking when the Cr-BM interneuron activated Cr-A neurons (n = 14). The Cr-BM neuron-induced EPSPs in the Cr-A neurons appeared only when corresponding spikes were observed in the Bc-PIN interneurons (n = 8; Fig. 5C). In addition, when the Bc-PIN interneurons were hyperpolarized and thus functionally removed from the network functioning, the Cr-A neuron response to the stimulation of the Cr-BM interneuron completely disappeared (n = 7). This provided strong evidence that Bc-PIN interneuron is indeed the element of the neural network that relays the excitatory inputs from the Cr-BM interneuron to the Cr-A neurons controlling opening of the skin folds and buccal cone protraction.
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GABA-immunoreactivity in the Clione central ganglia has been studied before (Arshavsky et al. 1993; Norekian 1999). Our detailed analysis of GABA immunoreactivity in the cerebral ganglia indicated that a pair of brightly stained immunoreactive cell bodies had the same position and body size as the Cr-BM interneurons. Each bilaterally symmetrical neuron with strong GABA immunoreactivity had body size of 25–30 µm and was located on the ventral side of the cerebral ganglia in the anterior region between head nerves N1 and N2 (n = 12; Fig. 7A). The following double-labeling experiments undoubtedly demonstrated that these GABA-immunoreactive neurons are Cr-BM interneurons (n = 6). One Cr-BM interneuron in each preparation, from the left or the right cerebral ganglion, was injected with neurobiotin and visualized with Texas Red (Fig. 7B). The same preparation was then processed for GABA immunoreactivity with the fluorescein-labeled secondary antibody (Fig. 7C). By switching filters in the same preparation, Cr-BM interneuron was identified as GABA-immunoreactive neuron. Texas Red and fluorescein had very distinct emission wavelengths and were visible only in their own set of filters, thus allowing complete separation of images and clear interpretation of data. Not only the cell body but also the entire morphological structure of the neurons could be seen through both filters and served as additional matching characteristic. This included a large axon entering the cerebro-buccal connective, and a group of thin processes innervating the neuropile of the ipsilateral cerebral ganglia (Fig. 7, B and C).
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). Incubation for 2–5 min in the 0.5 mM GABA solution blocked the Cr-BM neuron-induced EPSPs in the Bc-PIN and Bc-RP neurons presumably via occlusion of GABAergic receptors (n = 4). These experiments strongly supported the idea that Cr-BM interneurons are GABAergic cells.
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The Cr-BM interneuron produced a widespread effect in the buccal ganglia that was mostly centered on the activity of the neural networks controlling radula and hook movements. However, the buccal ganglia include neurons with other functional roles. One cell, designated Bc-L neuron, has been identified during this investigation as a putative motoneuron that controls closing of the skin folds over the mouth of Clione. The cell body of the bilaterally symmetrical Bc-L neuron was 20–25 µm in diameter and located in the posterior-medial part of each buccal ganglion (Fig. 10A). A single Bc-L neuron axon exited the ipsilateral buccal ganglion via the short hook nerve and crossed the entire muscular hook sac without any branching (n = 4; Fig. 10A). Then the axon crossed the connective tissue that linked the buccal mass with the head and entered the skin-fold region. Stimulation of the Bc-L neuron always produced a prominent closing of the skin folds in the semi-intact preparation (n = 9). Induced burst of spikes in the Cr-BM neuron triggered a prominent inhibition of the otherwise spontaneously active Bc-L neurons (n = 7; Fig. 10B). Each individual Cr-BM neuron spike produced a single IPSP in the Bc-L neuron that persisted in high-divalent solution suggesting monosynaptic connection (n = 5; Fig. 10C).
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DISCUSSION |
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In our previous study, we have described the phase-locked coordination between rhythmic activity of the hooks and radula, which both extract the prey from its shell and bring it to the gut (Malyshev and Norekian 2002). Clione does not bite small pieces from the prey during feeding but pulls the entire body of the prey from its shell, a process that occurs in 20–40 min (Lalli 1970; Lalli and Gilmer 1989; Wagner 1885). The radula and hooks take turns in pulling the prey out of the shell, moving in opposite phases of their protraction-retraction cycle, and keeping a constant extracting pressure (Malyshev and Norekian 2002). On the neuronal level, Bc-HP and Bc-RR neurons were always firing in phase with each other (Malyshev and Norekian 2002). The Bc-HR and Bc-RP neurons were also firing in phase, although there was a slight phase-shift in the Bc-HR neuron bursting, which allowed a brief co-activation between Bc-HR and Bc-HP neurons. In that investigation, we identified some of the neuronal mechanisms, which were responsible for the phase-locked coordination between hook and radula controlling motoneurons (Malyshev and Norekian 2002). The Bc-HP and Bc-RR neurons, which fire in one phase, were electrically coupled to each other; this explained their synchronous activity. The Bc-HR and Bc-RP neurons were not electrically coupled this allowed for the observed Bc-HR phase-shift and co-activation of the hook retractor and protractor neurons. The second mechanism of the phase-dependent coordination between hook and radula controlling neurons was reciprocal inhibitory connections found between different motoneurons. The Bc-HP neurons produced inhibitory inputs to the Bc-RP neurons briefly terminating their activity, while action potentials in the Bc-RP neurons, in turn, produced inhibition of the Bc-HP neurons (Malyshev and Norekian 2002).
In the current investigation, we significantly expand our understanding of the level of coordination between different feeding structures in Clione and the neuronal mechanisms of this coordination. The higher-order Cr-BM interneuron produced strong excitatory inputs to the neural networks that control hooks and radula rhythmic movements initiating their activity in quiescent preparations. In addition to this overall excitatory influence, Cr-BM interneuron produced fine-tuned, phase-specific coordination of individual radula and hook controlling motoneurons. The Cr-BM interneuron hyperpolarized both Bc-RR and Bc-HP motoneurons, which are active in one phase of the feeding rhythm. At the same time, Cr-BM interneuron depolarized Bc-RP motoneurons, Bc-PIN interneuron, and Bc-HR motoneurons, which are all active in the other phase. Moreover, two types of the Cr-BM neuron synaptic inputs to the Bc-HR motoneurons were responsible for or at least contributed to the phase-shift in the Bc-HR neuron bursting, which allowed a brief co-activation between Bc-HR and Bc-HP neurons. The initial Cr-BM neuron-induced fast IPSPs provided a delay in the Bc-HR neuron burst onset, whereas slow depolarization eventually over-rode the IPSPs and triggered a burst of activity, which lasted longer than Cr-BM neuron induced burst of spikes. This phase-shift in the Bc-HR neuron bursting created a brief period of co-activation of the Bc-HR and Bc-HP neurons that is presumably important for producing a fast and powerful protraction movement of the hooks (Malyshev and Norekian 2002). Co-activation of the functionally opposite motoneurons followed by the inhibition of one type of cells is a well-known mechanism for a fast and powerful movement (Heitler and Burrows 1977; Norekian and Satterlie 1993b). The previously described mechanisms of coordination between hooks and radula rhythmic movements were internal to their underlying neural networks: electrical coupling and reciprocal inhibition between hooks and radula controlling motoneurons (Malyshev and Norekian 2002). The Cr-BM interneuron influence is the external mechanism of this phase-locked coordination. In addition to initiating and controlling in the phase-dependent manner rhythmic activity of the radula and hook motoneurons, the Cr-BM interneuron also produced strong excitatory inputs to a large group of electrically coupled Cr-A neurons that control opening of the skin folds and hydraulic protraction of the buccal cones. Opening of the skin folds and buccal cone protraction are important components of the feeding behavior, which are present during the entire episode of feeding and responsible for capturing and holding the prey. In addition, if the skin folds are not open and buccal cones are not protracted, the hooks and radula cannot physically reach the prey. Thus Cr-BM interneuron apparently represents an important higher-order element of the feeding neural system with extensive coordinating influence on different participating neural networks.
Excitatory role of GABA in feeding behavior
One important characteristic of the Cr-BM interneurons that was uncovered during the current investigation was their GABAergic nature. It was demonstrated by the use of GABA antagonists, mimicking effect of exogenous GABA on postsynaptic neurons and double-labeling experiments, which showed that Cr-BM neurons are GABA-immunoreactive. GABA was originally known as inhibitory neurotransmitter. However, GABA-induced depolarizing effects were found in several neural systems (Beg and Jorgensen 2003; El-Beheiry and Puil 1990; Gallagher et al. 1978; Goldmakher and Moss 2000; Mercuri et al. 1991; Michelson and Wong 1991; Ogata 1987; Pfeiffer-Linn and Glantz 1989; Swensen et al. 2000). In some gastropod mollusks, GABA was found to function as an excitatory transmitter producing activation of the buccal feeding motor programs (Bravarenko et al. 2001; Richmond et al. 1993). An especially strong case for the excitatory role of GABA in the feeding system was made in Clione. Exogenous GABA produced activation not only of the buccal feeding neural network but also strong activation of the cerebral Cr-A neurons that control prey capture response of the buccal cones (Arshavsky et al. 1993; Norekian and Satterlie 1993c). The excitatory GABAergic Cr-Aint interneuron was later identified as a key element for the explosive and lasting discharge activity in the prey capture neural network (Norekian 1999). The excitatory responses in the Cr-A neurons induced by GABA had reverse potentials above zero and were sodium dependent (Norekian 1999). In this study, we have identified as GABAergic another important element of the feeding neural system with strong excitatory influence over several neural networks. Thus it appears that GABA acts as a potent excitatory transmitter in the feeding system of Clione.
Cerebro-buccal interneurons in gastropod mollusks
In most gastropod mollusks, the typical feeding response includes biting movements of jaws and rhythmic movements of the toothed radula that are controlled by the neural networks located in the buccal ganglia. In the several species of mollusks, a group of higher-order interneurons has been identified in the cerebral ganglia that project their axons to the buccal ganglia and influence activity of the feeding neural network. These cerebro-buccal interneurons have been identified in the carnivorous marine mollusk Pleurobranchaea (Gillette et al. 1982), the pond snail Lymnaea (McCrohan and Kyriakides 1989), and the land slug Limax (Delaney and Gelperin 1990). But the most detailed investigation of their functional role has been done in Aplysia, in which more than a dozen of the cerebro-buccal interneurons have been identified and studied (Hurwitz et al. 1999; Jing and Weiss 2001; Perrins and Weiss 1998; Rosen et al. 1991; Xin et al. 1999). Two of these cerebro-buccal interneurons have been identified as GABAergic: CBI-3 and CBI-11 neurons (Diaz-Rios et al. 1999; Jing et al. 2003; Wu et al. 2003). The CBI-11 interneuron produced a prominent excitatory effect on the buccal motor program and was capable of initiating feeding rhythm, whereas CBI-3 interneuron had regulatory influence (Jing et al. 2003; Wu et al. 2003). Identified in the current study Cr-BM interneuron in Clione is also a GABAergic cerebro-buccal interneuron. We believe that Cr-BM interneuron is homologous to the Aplysia GABAergic cerebro-buccal neurons, presumably to the CBI-11 neuron based on its morphology and physiological effect.
The transmitter nature, morphology, and general excitatory role in feeding behavior appear to be similar for these two presumably homologous cerebro-buccal interneurons, Cr-BM interneuron in Clione and CBI-11 interneuron in Aplysia. However, their specific connections and physiological effects are quite different and reflect the differences in the feeding habits of the animals. High food specialization in the carnivorous Clione is reflected in the appearance of two unique feeding structures (Lalli and Gilmer 1989). First, the buccal mass in Clione includes not only the radula and radula-controlling muscles but also two muscular hook sacs with numerous chitinous hooks that are used to pull the prey from its shell. And second, Clione acquired additional feeding structure for prey capture, buccal cones, which represent the protrusions of the buccal skin folds. These two new feeding structures are controlled by specific neural networks: hook controlling network in the buccal ganglia and a large group of buccal cone controlling Cr-A neurons in the cerebral ganglia. These feeding structures and underlying neural networks are absent in Aplysia. And the cerebro-buccal GABAergic Cr-BM interneuron in Clione carries a new functional role of activating not only the neural network that controls rhythmic movements of radula but also activation and phase-dependent coordination of the hook-controlling neural network and the neural network that controls the movements of the prey capture appendages, buccal cones.
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FOOTNOTES |
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Address for reprint requests and other correspondence: T. P. Norekian, Arizona State University, School of Life Sciences, Tempe, AZ 85287-4501 (E-mail: Tigran.Norekian{at}asu.edu)
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
|---|
Beg AA and Jorgensen EM. EXP-1 is an excitatory GABA-gated cation channel. Nat Neurosci 6: 1145–1152, 2003.[CrossRef][ISI][Medline]
Bravarenko NI, Ierusalimsky VN, Korshunova TA, Malyshev AY, Zakharov IS, and Balaban PM. Participation of GABA in establishing behavioral hierarchies in the terrestrial snail. Exp Brain Res 141: 340–348, 2001.[CrossRef][ISI][Medline]
Delaney K and Gelperin A. Cerebral interneurons controlling fictive feeding in Limax maximus. J Comp Physiol [A] 16: 297–326, 1990.
Diaz-Rios M, Suess E, and Miller MW. Localization of GABA-like imunoreactivity in the central nervous system of Aplysia californica. J Comp Neurol 413: 255–270, 1999.[CrossRef][ISI][Medline]
El-Beheiry H and Puil E. Unusual features of GABA responses in layers IV–V neurons of neocortex. Neurosci Lett 119: 83–85, 1990.[CrossRef][ISI][Medline]
Gallagher JP, Higashi H, and Nishi S. Characterization and ionic basis of GABA-induced depolarizations recorded in vitro from cat primary afferent neurons. J Physiol 275: 263–282, 1978.
Gillette R, Kovac MP, and Davis WJ. Control of feeding motor output by paracerebral neurons in brain of Pleurobranchaea californica. J Neurophysiol 47: 885–908, 1982.
Goldmakher GV and Moss RL. A subset of periglomerular neurons in the rat accessory olfactory bulb may be excited by GABA through a Na(+)-dependent mechanism. Brain Res 871: 7–15, 2000.[CrossRef][ISI][Medline]
Heitler WJ and Burrows M. The locust jump. I. The motor program. J. Exp Biol 66: 203–219, 1977.
Hurwitz I, Perrins R, Xin Y, Weiss KR, and Kupfermann I. C-PR neuron of Aplysia has differential effects on "feeding" cerebral interneurons, including myomodulin-positive CBI-12. J Neurophysiol 81: 521–534, 1999.
Jing J, Vilim FS, Wu J, Park J, and Weiss KR. Concerted GABAergic actions of Aplysia feeding interneurons in motor program specification. J Neurosci 23: 5283–5294, 2003.
Jing J and Weiss KR. Neural mechanisms of motor program switching in Aplysia. J Neurosci 21: 7349–7362, 2001.
Kosaka T, Nagatsu I, Wu JY, and Hama K. Use of high concentrations of glutaraldehyde for immunocytochemistry of transmitter-synthesizing enzymes in the central nervous system. Neuroscience 18: 975–990, 1986.[CrossRef][ISI][Medline]
Lalli CM. Structure and function of the buccal apparatus of Clione limacina (Phipps) with a review of feeding in Gymnosomatous pteropods. J Exp Mar Biol Ecol 4: 101–118, 1970.
Lalli CM and Gilmer RW. Pelagic Snails. The Biology of Holoplanktonic Gastropod Mollusks. Stanford, CA: Stanford Univ.Press, 1989, p. 167–213.
Malyshev AY and Norekian TP. Phase-Locked coordination between two rhythmically active feeding structures in the carnivorous mollusk Clione limacina. I. Motoneurons. J Neurophysiol 87: 2996–3005, 2002.
McCrohan CR and Kyriakides MA. Cerebral interneurones controlling feeding motor output in the snail Lymnaea stagnalis. J Exp Biol 147: 361–374, 1989.
Mercuri NB, Calabresi P, Stefani A, Stratta F, and Bernardi G. GABA depolarizes neurons in the rat striatum: an in vivo study. Synapse 8: 38–40, 1991.[CrossRef][ISI][Medline]
Michelson HB and Wong RKS. Excitatory synaptic responses mediated by GABAA receptors in the hippocampus. Science 253: 1420–1423, 1991.
Norekian TP. Prey capture phase of feeding behavior in the pteropod mollusc, Clione limacina: neuronal mechanisms. J Comp Physiol [A] 177: 41–53, 1995.[Medline]
Norekian TP. GABAergic excitatory synapses and electrical coupling sustain prolonged discharges in a prey capture neural network of Clione limacina. J Neurosci 19: 1863–1875, 1999.
Norekian TP and Satterlie RA. Cerebral neurons underlying prey capture movements in the pteropod mollusc, Clione limacina. I. Physiology morphology. J Comp Physiol [A] 172: 153–169, 1993a.[Medline]
Norekian TP and Satterlie RA. Co-activation of antagonistic motoneurons as a mechanism of high-speed hydraulic inflation of prey capture appendages in the pteropod mollusk, Clione limacina. Biol Bull 185: 240–247, 1993b.[Abstract]
Norekian TP and Satterlie RA. FMRFamide and GABA produce functionally opposite effects on prey-capture reactions in the pteropod mollusk, Clione limacina. Biol Bull 185: 248–262, 1993c.[Abstract]
Ogata N. 
-Aminobutyric acid (GABA) causes consistent depolarization of neurons in the guinea pig supraoptic nucleus due to an absence of GABAB recognition sites. Brain Res 403: 225–233, 1987.[CrossRef][ISI][Medline]
Perrins R and Weiss KR. Compartmentalization of information processing in an Aplysia feeding circuit interneuron through membrane properties and synaptic interactions. J Neurosci 18: 3977–3989, 1998.
Pfeiffer-Linn C, and Glantz RM. Acetylcholine and GABA mediate opposing actions on neuronal chloride channels in crayfish. Science 245: 1249–1251, 1989.
Richmond JE, Murphy AD, Lukowiak K, and Bulloch AGM. GABA regulates the buccal motor output of Helisoma by two pharmacologically distinct actions. J Comp Physiol [A] 174: 593–600, 1993.
Rosen SC, Teyke T, Miller MW, Weiss KR, and Kupfermann I. Identification and characterization of cerebral-to-buccal interneurons implicated in the control of motor programs associated with feeding in Aplysia. J Neurosci 11: 3630–3655, 1991.[Abstract]
Swensen AM, Golowasch J, Christie AE, Coleman MJ, Nusbaum MP, and Marder E. GABA and responses to GABA in the stomatogastric ganglion of the crab Cancer borealis. J Exp Biol 14: 2075–2092, 2000.
Wagner N. Die Wirbellosen des Weissen Meeres: Zoologische Forschungen an der Kuste des Solowetzkischen Meerbusens in den Sommermonaten der Jahre. Leipzig, Germany: Verlag Von Wilhelm Engelmann, 1885.
Wu J, Jing J, Diaz-Rios M, Miller MW, Kupfermann I, and Weiss KR. Identification of a GABA-containing cerebral-buccal interneuron-11 in Aplysia californica. Neurosci. Lett 341: 5–8, 2003.[CrossRef][ISI][Medline]
Xin Y, Hurwitz I, Perrins R, Evans CG, Alexeeva V, Weiss KR, and Kupfermann I. Actions of a pair of identified cerebral-buccal interneurons (CBI-8/9) in Aplysia that contain the peptide myomodulin. J Neurophysiol 81: 507–520, 1999.
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1 Hz failed to induce any significant increase in the EPSP amplitude.
