Impairment of the serotonergic neurons underlying reinforcement elicits extinction of the repeatedly reactivated context memory

Abstract

We analyzed changes in the activity of individually identifiable neurons involved in the networks underlying feeding and withdrawal behaviors in snails before, during, and after aversive learning in vitro. Responses to food in the “reinforcing” serotonergic neurons involved in withdrawal changed significantly after training, implying that these serotonergic cells participate in the reactivation of memory and are involved in the reconsolidation process. In behavioral experiments it was shown that impairment of the functioning of the serotonergic system with the selective neurotoxin 5,7-DiHT did not change the memory, when tested once, but resulted in a complete extinction of the contextual memory after repeated reactivation of memory. Conversely, the cued memory to a specific type of food was significantly reduced but still present. Thus, we conclude that it is only for the context memory, that participation of the “reinforcing” serotonergic neurons in memory retrieval may be the gate condition for the choice between extinction/reconsolidation.

Effects of Thryptophan Hydroxylase Blockade by P-Chlorophenylalanine on Contextual Memory Reconsolidation after Training of Different Intensity

“…It participates in a number of important physiological functions [81,82]. The participation of the serotonin system in animal cognition and behavior, in learning and memory attracts increasing attention [28,[83][84][85]. Therefore, the deregulation of the serotonergic system causes the pathogenesis of many psychiatric and neurological disorders [84,86].…”

“…Previously we found that PCPA at doses mentioned above induced the impairment of the formation of defensive conditioning in terrestrial snails as neurotoxins 5,7-DHT and 5,6-DHT [3], which occurred in the condition of the serotonin depletion in the nerve system [1][2][3]7,27,28,77,114,115].…”

“…The training procedure lasted 5 days, during training the snails did not receive food. The deprivation of food in invertebrate animals during the developing of conditioned reflexes is a standard technique, it is not associated with the metabolism of certain substances, but is determined by the need for an active state of the animal [28,60,61,78]. The procedure for "reminding" the training environment was to place the animals for 20 min in a training context of "on a ball".…”

“…It was shown that electrophysiological correlates of plasticity can be reproduced by applying 5-HT applications to the solution surrounding the central nervous system of mollusks [13][14][15][16][17][18][19][20][21]. On the other hand, the neurotoxic analogues of serotonin 5,6-and 5,7-dihydroxytryptamine (5, leading to the depletion of serotonin is widely used to study the role of the serotoninergic system in the formation of behavior and learning [1,7,[22][23][24][25][26][27][28].…”

“…It was found that neurotoxin 5,7-DHT blocked heterosynaptic facilitation in Aplysia [2], impaired the formation of the long-term sensitization in snail [3,32,33]. In behavioral experiments it was shown that the destruction of the functioning of the serotonergic system by neurotoxin 5,7-DHT did not change the original memory, but led to impairment of the memory after re-reactivation [28,34,35]. These results demonstrated the relevance of studying the dependence of long-term memory properties on the state of the serotonergic system.…”