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

Trudeau, Louis-Éric; Castellucci, Vincent F.

doi:10.1523/jneurosci.13-05-02126.1993

Cited by 35 publications

(15 citation statements)

References 37 publications

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“…Finally, we will need to determine the contribution of plasticity at interneuronal sites to learning, a subject that has been relatively unexplored in Aplysia, (but see Trudeau and Castellucci, 1993b;Tsau et al, 1994;Cleary et al, 1995;Frost and Kandel, 1995). A truly elephantine amount of work remains to be done.…”

Section: Resultsmentioning

confidence: 99%

The Cellular Mechanisms of Learning inAplysia:Of Blind Men and Elephants

Glanzman¹

2006

The Biological Bulletin

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Abstract. Until recently, investigations of the neurobiological substrates of simple forms of learning and memory in the marine snail Aplysia have focused mostly on plastic changes that occur within the presynaptic sensory neurons. Here, I summarize the results of recent studies that indicate that exclusively presynaptic processes cannot account for simple forms of learning in Aplysia. In particular, I present evidence that postsynaptic mechanisms play a far more important role in nonassociative learning in Aplysia than has been appreciated before now. Moreover, I describe recent data that suggests the intriguing hypothesis that the persistent, learning-induced changes in Aplysia sensory neurons might depend critically on postsynaptic signals for their induction. Finally, I discuss the potential applicability of this hypothesis to learning-related synaptic plasticity in the mammalian brain.

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Section: Resultsmentioning

confidence: 99%

The Cellular Mechanisms of Learning inAplysia:Of Blind Men and Elephants

Glanzman¹

2006

The Biological Bulletin

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“…A6 mimic responses of realistic amplitudes and durations in tail motor neurons. In the model the excitatory interneurons play an important role in transforming an amplitudecoded input into an amplitude-and duration-coded output that they deliver to the simulated tail motor neuron (see Byrne 1983;Frost et al 199 1;Trudeau and Castellucci 1992b for similar conclusions regarding the role of interneurons in the siphon-gill withdrawal reflex). In this way the model predicts that physiologically realistic modulation of synaptic connections between sensory neurons and LPI 17 neurons can exert a causal effect on both the magnitude and duration of the motor neuron response.…”

Section: Discussionmentioning

confidence: 99%

“…In recent studies of learning and memory in Aplysia, an increasing amount of emphasis has been placed on network properties rather than those of individual neurons. As men-tioned above, several of these studies have highlighted the role of interneurons in the control of the duration of reflexive responses (Byrne 1983;Frost et al 1988, 199 1;Lieb and Frost 1992;Trudeau and Castellucci 1992b). In addition, studies have focused on sites of plasticity other than the monosynaptic connection between sensory and motor neurons (Fischer and Carew 1993;Frost et al 1988;Lukowiak andColebrook 1988-1989;Trudeau and Castellucci 1992a,b;Xu et al 1992), the large number of neurons that may be involved in responses to stimulation of the skin (Zecevic et al 1989), and the roles of interneurons in inhibiting withdrawal responses (Blazis et al 1993;Fischer and Carew 1993;Hawkins et al 198 1;Mackey et al 1987;Small et al 1992;Xu et al 199 1).…”

Section: Studies Of Network Circuitry In Aplysiamentioning

confidence: 99%

The role of interneurons in controlling the tail-withdrawal reflex in Aplysia: a network model

White

Ziv

Cleary

et al. 1993

Journal of Neurophysiology

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1. The contributions of monosynaptic and polysynaptic circuitry to the tail-withdrawal reflex in the marine mollusk Aplysia californica were assessed by the use of physiologically based neural network models. Effects of monosynaptic circuitry were examined by the use of a two-layer network model with four sensory neurons in the input layer and one motor neuron in the output layer. Results of these simulations indicated that the monosynaptic circuit could not account fully for long-duration responses of tail motor neurons elicited by tail stimulation. 2. A three-layer network model was constructed by interposing a layer of two excitatory interneurons between the input and output layers of the two-layer network model. These interneurons had properties mimicking those of the recently described interneuron LP117, receiving excitatory input from pleural sensory neurons and evoking a biphasic excitatory postsynaptic potential (EPSP) in pedal motor neurons (Cleary and Byrne 1993). The three-layer model could account for long-duration responses in motor neurons. 3. Sensory neurons are a known site of plasticity in Aplysia. Synaptic plasticity was incorporated into the three-layer model by altering the magnitudes of conductance changes evoked in motor neurons and interneurons by presynaptic sensory neurons. In these simulations the excitatory interneurons converted an amplitude-coded input into an amplitude- and duration-coded output, allowing the three-layer network to support a large range of output amplitudes and durations. 4. Synaptic plasticity at more than one locus modified dramatically the input-output relationship of the three-layer network model. This feature gave the model redundancy in its plastic properties and points to the possibility of distributed memory in the circuitry mediating withdrawal reflexes in Aplysia. Multiple sites of control over the response of the network would likely allow a more diverse repertoire of responses.

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“…In some experiments, 75-l 00 PM d-tubocurarine was added to the bath in order to block spontaneous cholinergic synaptic potentials that interfered with the measurement of sensorimotor EPSPs. This treatment does not affect sensorimotor transmission or the effects of 5-HT (Trudeau and Castellucci, 1993b). The position of each of the sensory neurons was precisely mapped so that they could be reidentified with certainty the next day.…”

Section: Characterization Of the Agonist Responsementioning

confidence: 99%

Postsynaptic modifications in long-term facilitation in Aplysia: upregulation of excitatory amino acid receptors

Trudeau

Castellucci

1995

J. Neurosci.

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Long-term sensitization of the gill and siphon withdrawal in Aplysia is accompanied by facilitation of sensorimotor synaptic connections that depends on new protein synthesis. This phenomenon has been previously shown to involve presynaptic growth. At the postsynaptic level, a reorganization should occur to parallel the formation of new synaptic contacts. We show here that 24 hr following an application of 5-HT, which produces long-term synaptic facilitation (LTF), the response of the motoneuron to an excitatory amino acid agonist of the synaptic receptors is increased. General inhibition of protein synthesis with anisomycin blocks this enhancement. Inhibiton of protein synthesis limited to the postsynaptic neuron by intracellular injection of gelonin, a ribosome-inactivating toxin, also blocks the increase in the response to the agonist but fails to block 24 hr LTF. These results are compatible with a model of LTF that involves coordinate pre- and postsynaptic changes. The latter may include an upregulation of functional postsynaptic receptors. These may not be initially required for LTF measured at a 24 hr time point, but could become necessary for later stages of LTF. An increase in the number of functional postsynaptic receptors in a reserve pool may also prime the postsynaptic neuron for subsequent learning-associated plasticity.

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

Cited by 35 publications

References 37 publications

The Cellular Mechanisms of Learning inAplysia:Of Blind Men and Elephants

The Cellular Mechanisms of Learning inAplysia:Of Blind Men and Elephants

The role of interneurons in controlling the tail-withdrawal reflex in Aplysia: a network model

Postsynaptic modifications in long-term facilitation in Aplysia: upregulation of excitatory amino acid receptors

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