Learning phenomena in the giant neurons of the snail (Helix pomatia) (original) (raw)

Balanced plasticity and stability of the electrical properties of a molluscan modulatory interneuron after classical conditioning: a computational study

Frontiers in …, 2010

The Cerebral Giant Cells (CGCs) are a pair of identified modulatory interneurons in the Central Nervous System of the pond snail Lymnaea stagnalis with an important role in the expression of both unconditioned and conditioned feeding behavior. Following single-trial food-reward classical conditioning, the membrane potential of the CGCs becomes persistently depolarized. This depolarization contributes to the conditioned response by facilitating sensory cell to command neuron synapses, which results in the activation of the feeding network by the conditioned stimulus. Despite the depolarization of the membrane potential, which enables the CGGs to play a key role in learning-induced network plasticity, there is no persistent change in the tonic firing rate or shape of the action potentials, allowing these neurons to retain their normal network function in feeding. In order to understand the ionic mechanisms of this novel combination of plasticity and stability of intrinsic electrical properties, we first constructed and validated a Hodgkin-Huxley-type model of the CGCs. We then used this model to elucidate how learning-induced changes in a somal persistent sodium and a delayed rectifier potassium current lead to a persistent depolarization of the CGCs whilst maintaining their firing rate. Including in the model an additional increase in the conductance of a high-voltage-activated calcium current allowed the spike amplitude and spike duration also to be maintained after conditioning. We conclude therefore that a balanced increase in three identified conductances is sufficient to explain the electrophysiological changes found in the CGCs after classical conditioning.

Adaptation in Helix pomatia neurons

Comparative Biochemistry and Physiology Part A: Physiology, 1987

l. Spike frequency adaptation has been studied on neurons of Helix pomatia subesophageal ganglia and interpreted by means of a behavioural model describing the phenomenon in neurons either silent or autorhythmic at rest.

Associative learning phenomena in the snail (Helix aspersa): Conditioned inhibition

Learning & Behavior, 2012

Two experiments using garden snails (Helix aspersa) showed conditioned inhibition using both retardation and summation tests. Conditioned inhibition is a procedure by which a stimulus becomes a predictor of the absence of a relevant event-the unconditioned stimulus (US). Typically, conditioned inhibition consists of pairings between an initially neutral conditioned stimulus, CS 2 , and an effective excitatory conditioned stimulus, CS 1 , in the absence of the US. Retardation and summation tests are required in order to confirm that CS 2 has acquired inhibitory properties. Conditioned inhibition has previously been found in invertebrates; however, these demonstrations did not use the retardation and summation tests required for an unambiguous demonstration of inhibition, allowing for alternative explanations. The implications of our results for the fields of comparative cognition and invertebrate physiological models of learning are discussed.

Electrophysiological characteristics of feeding-related neurons after taste avoidance Pavlovian conditioning in Lymnaea stagnalis

BIOPHYSICS, 2014

Taste avoidance conditioning (TAC) was carried out on the pond snail, Lymnaea stagnalis. The conditional stimulus (CS) was sucrose which elicits feeding behavior; while the unconditional stimulus (US) was a tactile stimulus to the head which causes feeding to be suppressed. The neuronal circuit that drives feeding behavior in Lymnaea is well worked out. We therefore compared the physiological characteristics on 3 classes of neurons involved with feeding behavior especially in response to the CS in conditioned vs. control snails. The cerebral giant cell (CGC) modulates feeding behavior, N1 medial neuron (N1M) is one of the central pattern generator neurons that organizes feeding behavior, while B3 is a motor neuron active during the rasp phase of feeding. We found the resting membrane potential in CGC was hyperpolarized significantly in conditioned snails but impulse activity remained the same between conditioned vs. control snails. There was, however, a significant increase in spontaneous activity and a significant depolarization of N1M's resting membrane potential in conditioned snails. These changes in N1M activity as a result of training are thought to be due to withdrawal interneuron RPeD11 altering the activity of the CGCs. Finally, in B3 there was: 1) a significant decrease in the amplitude and the frequency of the post-synaptic potentials; 2) a significant hyperpolarization of resting membrane potential in conditioned snails; and 3) a disappearance of bursting activity typically initiated by the CS. These neuronal modifications are consistent with the behavioral phenotype elicited by the CS following conditioning.

The role of cGMP in the extinction of the reactions of identified neurons of the edible snail in response to acetylcholine

Neuroscience and Behavioral Physiology, 1990

The possible role of cGMP in the regulation of the extinction of the reactions of the RPa4, RPa3, and LPa3 neurons of the edible snail in response to acetylcholine (ACh), applied rhythmically to the soma of the neuron by means of microiontophoresis, has been investigated. It was demonstrated that activators of guanylate cyclase which increased the level of cGMP in the cell, namely, sodium nitroprusside and sodium azide (5·104 103 mole/liter), when applied intracellularly, intensify the extinction of inward transmembrane current and of depolarization of the membrane in response to ACh. The hypothesis of the participation of cGMP-dependent phosphorylation of membrane proteins in the regulation of the rate of development, depth, and duration of short-lived plasticity of the cholinoreceptors of the neuron is proposed.

Action potential bursts in central snail neurons elicited by paeonol: roles of ionic currents

2010

The role of ionic currents on procaine-elicited action potential bursts was studied in an identifiable RP1 neuron of the African snail, Achatina fulica Ferussac, using the two-electrode voltage clamp method. The RP1 neuron generated spontaneous action potentials and bath application of procaine at 10 mM reversibly elicited action potential bursts in a concentration-dependent manner. Voltage clamp studies revealed that procaine at 10 mM decreased [1] the Ca 2+ current, [2] the Na + current, [3] the delayed rectifying K + current (IKD), and [4] the fast-inactivating K + current (I A ). Action potential bursts were not elicited by 4-aminopyridine (4-AP), an inhibitor of I A , whereas they were seen after application of tetraethylammonium chloride (TEA), a blocker of the I K(Ca) and I KD currents, and tacrine, an inhibitor of I KD . Pretreatment with U73122, a phospholipase C inhibitor, blocked the action potential bursts elicited by procaine. U73122 did not affect the I KD of the RP1 neuron; however, U73122 decreased the inhibitory effect of procaine on the I KD . Tacrine decreased the TEA-sensitive I KD of RP1 neuron but did not significantly affect the I A . Tacrine also successfully induced action potential bursts in the RP1 neuron. It is concluded that the inhibition on the I KD is responsible for the generation of action potential bursts in the central snail RP1 neuron. Further, phospholipase C activity is involved in the procaineelicited I KD inhibition and action potential bursts.

Electrophysiological characteristics of peripheral neurons and their synaptic connections in the intestinal nerve of Helix pomatia L

Comparative Biochemistry and Physiology Part A: Physiology, 1985

Nerve cells in the intestinal nerve of Helix pomutiu were studied, with respect to their localization, light microscopic morphology and electrophysiological properties, in a semi-intact preparation consisting of the ganglionic ring, intestinal nerve trunk and heart-kidney complex. 2. After retrograde labelling with Co 2+ through the cardiac nerve, a population of nerve cell bodies, 30-40 lm in diameter, can be observed around the first bifurcation of the intestinal nerve trunk and along the finer nerve branches. In addition, a few large elongated neuronal perikarya, 80-90 pm in length, are present at the base of the branching point of the intestinal nerve trunk. 3. On the basis of synaptic responses evoked either by the electrical stimulation of the peripheral nerves running to the central ganglia or by the tactile stimulation of the heart and kidney, the nerve cells could be divided into three groups. 4. Blockage of the synaptic transmission in the central nervous system with a high Mg2+, low Ca*+-containing medium decreases or blocks the responses of the peripheral neurons evoked by the stimulation of peripheral nerves and peripheral organs. This observation suggests that the neuronal elements of the CNS are in a presynaptic position to, and may have a facilitatory influence on, the neurons located in the intestinal nerve. 5. The present results support our previous suggestion that the peripheral neurons located in the intestinal nerve trunk may participate in the integrative processes contributing to the control of visceral functions. pomatia, having a functional relation to cardiorespiratory activity. In Neurobiology of Invertebrates, Gastropoda Brain (Edited by Sallnki J.), pp. 615-627. Akadbmiai Kiadb, Budapest.

Coupled neuronal oscillators in the snail Lymnaea stagnalis: endogenous cellular properties and network interactions

Journal of Experimental Biology

The role of endogenous cellular properties and network interactions due to electrotonic coupling were investigated in two bilateral populations of 2–7 peripheral neurones (‘Peripheral Bursters’) in the snail Lymnaea stagnalis. 1. These cells are endogenously capable of bursting. Their burst frequency does not depend on the level of steady membrane polarization. Short hyperpolarizing current pulses injected during the bursting cycle induce phase advance and no phase delay in subsequent cycles, the phase advance being a function of the phase of stimulus application. Phase response and inter-burst interval curves have been constructed for short hyperpolarizing current pulses. Their shape depends on the intensity and sign of tonically injected current. This property of Peripheral Bursters is one reason for the independence of period duration from membrane polarization. 2. Coordination of burst activity of Peripheral Bursters has been studied as a function of coupling strength: whereas h...

Effects of rolipram on induction of action potential bursts in central snail neurons

Experimental Neurology, 2005

Effects of rolipram, a selective inhibitor of phosphodiesterases (PDE) IV, on induction of action potential bursts were studied pharmacologically on the RP4 central neuron of the giant African snail (Achatina fulica Ferussac). Oscillations of membrane potential bursts were elicited by rolipram and forskolin. The bursts of potential elicited by rolipram were not inhibited after administration with (a) calcium-free solution, (b) high-magnesium solution (30 mM) or (c) U73122. However, the bursts of potential elicited by rolipram were inhibited by pretreatment with KT-5720 (10 microM). Voltage-clamp studies revealed that rolipram decreased the total inward current and steady-state outward currents of the RP4 neuron. The negative slope resistance (NSR) was not detectable in control or rolipram treated RP4 neurons. TEA elicited action potential bursts and an NSR at membrane potential between -50 mV and -30 mV. It is suggested that the bursts of potential elicited by rolipram were not due to (1) synaptic effects of neurotransmitters; (2) NSR of steady-state I-V curve; (3) phospholipase activity of the neuron. The rolipram-elicited bursts of potential were dependent on the phosphodiesterases inhibitory activity and the cAMP signaling pathway in the neuron.