Physiological and biochemical properties of neuromuscular transmission between identified motoneurons and gill muscle in Aplysia.

Carew, TJ; Pinsker, H. M.; Rubinson, Kenneth A.; Kandel, ER

doi:10.1152/jn.1974.37.5.1020

Cited by 115 publications

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“…The gill potential amplitude followed the EJPs in a linear manner and is an accurate representation of the EJP amplitude. Our observations on EJPs are in general agreement with earlier studies (14). We observed EJPs with unfacilitated amplitudes from 2 to 7 mV and facilitated amplitudes of up to 20 mV from 45 impalements (six preparations) of efferent vein longitudinal muscle fibers with resting potentials of 60-70 mV.…”

supporting

confidence: 93%

“…If habituation is caused solely by synaptic depression at sensory-motor synapses (9,13), the firing of the motor neurons should parallel the evoked gill withdrawal because these neurons synapse directly on gill muscles and are reported to produce temporally stable nondecrementing gill withdrawal (10,14). However, it was shown that the neuron-gill muscle synapses showed pronounced facilitation (14).…”

mentioning

confidence: 99%

“…* The effect of antecedent activity in LDG1 prior to P2 is similar to the effect of a dishabituatory stimulus because it promotes firing in motor neurons and the facilitation of EJPs. Thus, the gill withdrawal evoked by a spike train during a habituation depends upon the frequency of the evoked spikes (because of the frequency-dependent facilitation of the gill muscle EJPs) and the facilitated * Selective current pulses applied to motor neurons at constant intervals (10 or 30 see) may cause relatively stable gill withdrawal (14 (P1, P2, P3) while gill potentials (G-P), gill withdrawal (G-T), and LDG1 and L7 were recorded. L7 was unaffected by firing LDG1, as found by others (11).…”

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Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Jacklet¹,

Rine²

1977

Proc. Natl. Acad. Sci. U.S.A.

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The gill withdrawal reflex of Aplysia has been used as a model for studying the neuronal mechanisms of habituation, a behavioral plasticity. We have assessed the contribution of neuromuscular facilitation, an elementary synaptic plasticity, during habituation of the reflex by recording gill muscle potentials, which we show are caused by excitatory junctional potentials. These potentials show systematic frequency-dependent changes in amplitude. The gill withdrawal evoked by central motor neuron firing during each habituation trial is determined by facilitation of the excitatory junctional potentials during the trial and the facilitated state of the initial excitatory junctional potential in a trial, determined by neuron activity prior to the trial. The neuromuscular junctions, therefore, act like a frequency-dependent amplifier of central motor activity. They are fully responsive to the dynamic changes of motor neuron firing that occurs during habituation and especially after dishabituation.The neural correlates of habituation have been extensively studied in three invertebrate preparations, the crayfish (Procambaxrus) (1-3), the locust (Schistocerca) (4), and the sea hare (Apiysia). Habituation, the decrement of a behavioral response with repeated stimulation and its restoration or dishabituation by a novel stimulus, can be studied in these preparations at the level of synaptic communication between neurons. In these animals, and possibly in vertebrates (5), homosynaptic depression at central neuronal synapses has been identified as a mechanism of habituation (1-4, 6, 7).In Aplysia the reflex withdrawal of the gill evoked by siphon stimulation has been used as a model for the study of habituation (7-9). Several central motor neurons participate in this reflex, and studies of motor neuron L7 have shown that it receives excitatory postsynaptic potential (EPSP) input from a cluster of central sensory neurons (10-12). These EPSPs decrease in amplitude with successive stimuli and therefore, as a consequence of a decrease in the number of quanta of transmitter released (13) at the sensory-motor chemical synapses, homosynaptic depression has been proposed as the mechanism of habituation of the reflex (7, 9). The train of action potentials evoked by synaptic input to neuron L7 during behavioral habituation and dishabituation has been shown (9) but the firing of other major motor neurons (LDG1 and LDG2) has not. The firing of L7 decreases slowly during behavioral habituation of the gill and recovers slowly after dishabituation (9). If habituation is caused solely by synaptic depression at sensory-motor synapses (9, 13), the firing of the motor neurons should parallel the evoked gill withdrawal because these neurons synapse directly on gill muscles and are reported to produce temporally stable nondecrementing gill withdrawal (10, 14). However, it was shown that the neuron-gill muscle synapses showed pronounced facilitation (14).We examined the possibility that changes in the efficacy of gill neuromuscular junction...

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confidence: 93%

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confidence: 99%

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confidence: 99%

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Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Jacklet¹,

Rine²

1977

Proc. Natl. Acad. Sci. U.S.A.

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“…Because the same results were obtained with direct stimulation of the siphon nerve, this issue does not appear to have been a problem under our experimental conditions. The semi-intact preparations did not include an intact ctenidial (genital) nerve or an intact peripheral pathway, which are known to also play a role in the mediation of evoked gill contractions in the intact animal (Carew et al, 1974;Lukowiak and Peretz, 1977). We have restricted our analysis to the central component of the GSWR network and to its output through the branchial nerve (gill component).…”

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confidence: 99%

Functional uncoupling of inhibitory interneurons plays an important role in short-term sensitization of Aplysia gill and siphon withdrawal reflex

Trudeau

Castellucci

1993

J. Neurosci.

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Attempts to explain learning-associated potentiation of synaptic transmission in model systems such as withdrawal reflexes in the mollusk Aplysia or the hippocampus of vertebrates have focused on the mechanisms by which transmitter release is increased in the principal elements of the circuit. Increased transmission in neuronal networks such as the gill and siphon withdrawal reflex (GSWR) of Aplysia may, however, also be caused by a decrease of transmitter release by inhibitory interneurons. The importance and function of cholinergic inhibitory transmission in the GSWR network were investigated. Central application of the nicotinic cholinergic antagonist d-tubocurarine (d- TC) considerably potentiated gill contractions, evoked either by nerve stimulation or by tactile stimulation of the siphon. Compound EPSPs evoked in motoneurons upon siphon nerve stimulation were also significantly prolonged following application of d-TC, but were unaffected by hexamethonium, a blocker of excitatory ACh receptors in Aplysia. Recordings from excitatory interneurons showed that they received excitation followed by powerful inhibitory input upon stimulation of the siphon nerve. Application of d-TC completely blocked this rapid inhibition, thus prolonging the compound EPSPs evoked in the interneurons. These effects were obtained at a concentration of d-TC (100 microM) that almost totally blocked fast inhibitory cholinergic transmission, but was without effect on monosynaptic connections between sensory neurons and motoneurons of the reflex. Facilitation of (1) compound EPSCs in motoneurons and (2) evoked excitatory interneuronal firing was reduced in preparations already disinhibited by pretreatment with d-TC. Facilitation of sensory-motor synapses, however, was not reduced in the presence of d-TC, indicating that facilitatory interneurons are still activated under cholinergic blockade. These data show that transmission through the GSWR neuronal network is gated by a feedback inhibitory mechanism. They also suggest that a reduction of cholinergic inhibition onto excitatory interneurons may be a mechanism through which transmission within the GSWR network is increased during various forms of learning, such as sensitization. These data place new emphasis on the important role of inhibitory interneurons in determining the plastic properties of neuronal networks, in both invertebrates and vertebrates.

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“…The ganglion cells of Aplysia can serve as useful models for the study of interaction at isolated receptors, since many cells have been identified including various kinds of postsynaptic receptors such as for acetylcholine (ACh), histamine (HA), r-aminobutyric acid (GABA), dopamine (DA), and serotonin (5-HT). There is a certain amount of evidence that ACh, 5-HT, HA, and DA are natural neurotransmitters in this system (GILLER and SCHWARTZ, 1971;CAREW et al, 1974;GERSCHENFELD et al, 1978;WEINREICH, 1977;SWANN et al, 1982a, b). Two types of DA receptors have been identified in the ganglion cells of Aplysia (ASHCER, 1972); one is the excitatory or D-type which exhibits a depolarizing response to DA, and the other is the inhibitory or H-type which responds to DA with a marked hyperpolarization associated with an increase in membrane conductance.…”

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confidence: 99%

Blocking effect of serotonin on inhibitory dopamine receptor activity of Aplysia ganglion cells.

Shozushima

1984

Jpn.J.Physiol

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1) The abdominal ganglion of Aplysia includes neurons with a characteristic dopamine (DA) receptor, the activation of which induces a marked hyperpolarization with a specific increase in the permeability of the membrane to KtThe DA receptor of this type is called the "H K-type." 2) A 2-min exposure to 1,IM serotonin (5-HT) had little effect on the resting membranes with the receptor of HK-type, but significantly depressed the responses to 10 µM DA. The depressing effect of 5-HT on this type of response was completely reversible after a 15-min washing with normal artificial Aplysia blood. 3) Lineweaver-Burke type plotting of the DA-induced responses showed a systematic shift of the straight lines when the concentration of 5-HT was increased; the slope of the line became steeper but the intercept on the ordinate remained unchanged. 4) The dose-inhibition curves, in which relative responses to a given [DA] were plotted against log [5-HT], showed a parallel shift toward the right when the concentration of DA increased. 5) These findings suggest that 5-HT competes with DA for common binding sites at the DA receptor of HK-type, and that the blockade is not due to the interaction of 5-HT with K+-channels in the receptor membrane. 6) The effect of other indole derivatives suggests that the DA receptor of HK-type includes anionic and cationic sites to which the NH2 group and 5-HO group of 5-HT could specifically bind, thus exhibiting competitive blockade.

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Physiological and biochemical properties of neuromuscular transmission between identified motoneurons and gill muscle in Aplysia.

Cited by 115 publications

References 0 publications

Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Functional uncoupling of inhibitory interneurons plays an important role in short-term sensitization of Aplysia gill and siphon withdrawal reflex

Blocking effect of serotonin on inhibitory dopamine receptor activity of Aplysia ganglion cells.

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