scholarly journals Interneuronal mechanisms underlying a learning-induced switch in a sensory response that anticipates changes in behavioural outcomes

2020 ◽  
Author(s):  
Zsolt Pirger ◽  
Zita László ◽  
Souvik Naskar ◽  
Michael O’Shea ◽  
Paul R. Benjamin ◽  
...  

ABSTRACTHow an animal responds to a particular sensory stimulus will to a great extent depend on prior experience associated with that stimulus. For instance, aversive associative learning may lead to a change in the predicted outcomes, which suppresses the behavioural response to an otherwise rewarding stimulus. However, the neuronal mechanisms of how aversive learning can result in the suppression of even a vitally important innate behaviour is not well understood. Here we used the model system of Lymnaea stagnalis to address the question of how an anticipated aversive outcome can alter the behavioural response to a previously effective feeding stimulus. We found that aversive classical conditioning with sucrose as the CS (conditioned stimulus) and strong touch as the aversive US (unconditioned stimulus) reverses the decision so that the same salient feeding stimulus inhibits feeding, rather than activating it. Key to the understanding of the neural mechanism underlying this switch in the behavioural response is the PlB (pleural buccal) extrinsic interneuron of the feeding network whose modulatory effects on the feeding circuit inhibit feeding. After associative aversive training, PlB is excited by sucrose to reverse its effects on the feeding response. Aversive associative learning induces a persistent change in the electrical properties of PlB that is both sufficient and necessary for the switch in the behavioural output. In addition, the strong touch used as the US during the associative training protocol can also serve as a sensitizing stimulus to lead to an enhanced defensive withdrawal response to a mild touch stimulus. This non-associative effect of the strong touch is probably based on the facilitated excitatory output of a key identified interneuron of the defensive withdrawal network, PeD12.

2013 ◽  
Vol 91 (6) ◽  
pp. 405-412 ◽  
Author(s):  
E. Ito ◽  
S. Kojima ◽  
K. Lukowiak ◽  
M. Sakakibara

The neural circuitry comprising the central pattern generator (CPG) that drives feeding behavior in the great pond snail (Lymnaea stagnalis (L., 1758)) has been worked out. Because the feeding behavior undergoes associative learning and long-term memory (LTM) formation, it provides an excellent opportunity to study the causal neuronal mechanisms of these two processes. In this review, we explore some of the possible causal neuronal mechanisms of associative learning of conditioned taste aversion (CTA) and its subsequent consolidation processes into LTM in L. stagnalis. In the CTA training procedure, a sucrose solution, which evokes a feeding response, is used as the conditioned stimulus (CS) and a potassium chloride solution, which causes a withdrawal response, is used as the unconditioned stimulus (US). The pairing of the CS–US alters both the feeding response of the snail and the function of a pair of higher order interneurons in the cerebral ganglia. Following the acquisition of CTA, the polysynaptic inhibitory synaptic input from the higher order interneurons onto the feeding CPG neurons is enhanced, resulting in suppression of the feeding response. These changes in synaptic efficacy are thought to constitute a “memory trace” for CTA in L. stagnalis.


2002 ◽  
Vol 205 (8) ◽  
pp. 1171-1178 ◽  
Author(s):  
Susan Sangha ◽  
Chloe McComb ◽  
Andi Scheibenstock ◽  
Christine Johannes ◽  
Ken Lukowiak

SUMMARY A continuous schedule of reinforcement (CR) in an operant conditioning procedure results in the acquisition of associative learning and the formation of long-term memory. A 50 % partial reinforcement (PR) schedule does not result in learning. The sequence of PR—CR training has different and significant effects on memory retention and resistance to extinction. A CR/PR schedule results in a longer-lasting memory than a PR/CR schedule. Moreover,the memory produced by the CR/PR schedule is resistant to extinction training. In contrast, extinction occurs following the PR/CR schedule.


2000 ◽  
Vol 53 (2b) ◽  
pp. 173-187 ◽  
Author(s):  
Catherine E. Myers ◽  
Lindsay M. Oliver ◽  
Stacey G. Warren ◽  
Mark A. Gluck

Learning that one cue (CS) predicts a second, salient cue (US) can often be slowed by prior exposure to one or both stimuli. In animals, CS-US learning is more strongly retarded following uncorrelated exposure to both CS and US than following exposure to the US alone. In this paper we present several studies showing a similar effect in humans, using a computer-based task. Experiments 1 and 2 used a between-groups design and demonstrated a strong CS/US exposure effect, whether or not the US was signalled by a neutral cue during exposure. Experiment 3 demonstrated similar effects using a within-subjects design. Overall, these results are consistent with several theoretical interpretations and suggest that uncorrelated CS/US exposure leads to a robust retardation of subsequent CS-US learning in humans.


2002 ◽  
Vol 88 (4) ◽  
pp. 1584-1591 ◽  
Author(s):  
Andi Scheibenstock ◽  
Darin Krygier ◽  
Zara Haque ◽  
Naweed Syed ◽  
Ken Lukowiak

The cellular basis of long-term memory (LTM) storage is not completely known. We have developed a preparation where we are able to specify that a single identified neuron, Right Pedal Dorsal 1 (RPeD1), is a site of LTM formation of associative learning in the pond snail, Lymnaea stagnalis. We demonstrated this by ablating the soma of the neuron but leaving behind its functional primary neurite, as evidenced by electrophysiological and behavioral analyses. The soma-less RPeD1 neurite continues to be a necessary participant in the mediation of aerial respiratory behavior, associative learning, and intermediate-term memory (ITM); however, LTM cannot be formed. However, if RPeD1's soma is ablated after LTM consolidation has occurred, LTM can still be accessed. Thus the soma of RPeD1 is a site of LTM formation.


1996 ◽  
Vol 13 (6) ◽  
pp. 803-812 ◽  
Author(s):  
Satoshi Kojima ◽  
Mari Yamanaka ◽  
Yutaka Fujito ◽  
Etsuro Ito

1991 ◽  
Vol 158 (1) ◽  
pp. 63-95 ◽  
Author(s):  
G. P. Ferguson ◽  
P. R. Benjamin

Two muscle systems mediated the whole-body withdrawal response of Lymnaea stagnalis: the columellar muscle (CM) and the dorsal longitudinal muscle (DLM). The CM was innervated by the columellar nerves and contracted longitudinally to shorten the ventral head-foot complex and to pull the shell forward and down over the body. The DLM was innervated by the superior and inferior cervical nerves and the left and right parietal nerves. During whole-body withdrawal, the DLM contracted synchronously with the CM and shortened the dorsal head-foot longitudinally. The CM and the DLM were innervated by a network of motoneurones. The somata of these cells were located in seven ganglia of the central nervous system (CNS), but were especially concentrated in the bilaterally symmetrical A clusters of the cerebral ganglia. The CM was innervated by cells in the cerebral and pedal ganglia and the DLM by cells in the cerebral, pedal, pleural and left parietal ganglia. Individual motoneurones innervated large, but discrete, areas of muscle, which often overlapped with those innervated by other motoneurones. Motoneuronal action potentials evoked one-for-one non-facilitating excitatory junction potentials within muscle fibres. No all-or-nothing action potentials were recorded in the CM or DLM, and they did not appear to be innervated by inhibitory motoneurones. The whole network of motoneurones was electrotonically coupled, with most cells on one side of the CNS strongly coupled to each other but weakly coupled to cells on the contralateral side of the CNS. This electrotonic coupling between motoneurones is probably important in producing synchronous contraction of the CM and DLM when the animal retracts its head-foot complex during whole-body withdrawal.


1988 ◽  
Vol 140 (1) ◽  
pp. 273-285 ◽  
Author(s):  
K. Lukowiak ◽  
E. Colebrook

In a semi-intact preparation of Aplysia californica Cooper, classical conditioning training leads to changes in the synaptic strength at the sensory-motor neurone synapse. However, these changes are neither necessary nor sufficient to bring about the observed behavioural changes of the gill withdrawal reflex. We therefore tested whether the ability of a gill motor neurone to elicit a gill withdrawal response was altered following classical conditioning training of the reflex. We found that following classical conditioning training, the ability of a gill motor neurone to elicit a gill withdrawal response was significantly potentiated. In addition, in control preparations which did not receive classical conditioning training, the ability of a gill motor neurone to elicit a gill response was decreased. Thus, associative learning of this reflex appears to involve alteration in neuronal activity at loci distal to the sensory-motor neurone synapse.


2003 ◽  
Vol 6 (2) ◽  
pp. 155-167 ◽  
Author(s):  
Luis Aguado

Current knowledge on the neuronal substrates of Pavlovian conditioning in animals and man is briefly reviewed. First, work on conditioning in aplysia, that has showed amplified pre-synaptic facilitation as the basic mechanism of associative learning, is summarized. Then, two exemplars of associative learning in vertebrates, fear conditioning in rodents and eyelid conditioning in rabbits, are described and research into its neuronal substrates discussed. Research showing the role of the amygdala in fear conditioning and of the cerebellum in eyelid conditioning is reviewed, both at the circuit and cellular plasticity levels. Special attention is given to the parallelism suggested by this research between the neuronal mechanisms of conditioning and the principles of formal learning theory. Finally, recent evidence showing a similar role of the amygdala and of the cerebellum in human Pavlovian conditioning is discussed.


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