Neural Correlates of Pavlovian Conditioning in Components of the Neural Network Supporting Ciliary Locomotion inHermissenda

Abstract

Pavlovian conditioning in Hermissenda consists of pairing light, the conditioned stimulus (CS) with activation of statocyst hair cells, the unconditioned stimulus (US). Conditioning produces CS-elicited foot shortening and inhibition of light-elicited locomotion, the two conditioned responses (CRs). Conditioning correlates have been identified in the primary sensory neurons (photoreceptors) of the CS pathway, interneurons that receive monosynaptic input from identified photoreceptors, and putative pedal motor neurons. While cellular mechanisms of acquisition produced by the synaptic interaction between the CS and US pathways are well-documented, little is known about the mechanisms responsible for the generation or expression of the CR. Here we show that in conditioned animals light reduced tonic firing of ciliary activating pedal neurons (VP1) below their pre-CS baseline levels. In contrast, pseudorandom controls expressed a significant increase in CS-elicited tonic firing of VP1 as compared to pre-CS baseline activity. Identified interneurons in the visual pathway that have established polysynaptic connections with VP1 were examined in conditioned animals and pseudorandom controls. Depolarization of identified type I e interneurons with extrinsic current elicited a significant increase in IPSPs recorded in VP1 pedal neurons of conditioned animals as compared with pseudorandom controls. Conditioning also enhanced intrinsic excitability of type I e interneurons of conditioned animals as compared to pseudorandom controls. Light evoked a modest increase in IPSP frequency in VP1 of conditioned preparations and a significant decrease in IPSP frequency in VP1 of pseudorandom controls. Our results show that a combination of synaptic facilitation and intrinsic enhanced excitability in identified components of the CS pathway may explain light-elicited inhibition of locomotion in conditioned animals.Pavlovian conditioning in Hermissenda results in conditioned stimulus (CS)-elicited inhibition of phototaxis (Crow and Alkon 1978;Crow and Offenbach 1983) and CS-elicited foot contraction (Lederhendler et al. 1986). While these two motor acts appear dissimilar, inhibition of CS-elicited ciliary locomotion and CS-elicited foot contraction may synergistically interact to contribute to the inhibition of phototactic behavior observed in conditioned animals. While some progress has been made in the identification of foot contraction motor neurons (Goh and Alkon 1984) and cellular neurophysiological correlates of conditioning in a contractile pedal motor neuron (Goh et al. 1985), little is known regarding cellular plasticity in the neural network supporting ciliary locomotion in conditioned Hermissenda. Recently, pedal neurons activating cilia on the anterior foot have been identified and synaptic connections between type I, II, and III interneurons and VP1 ciliary activating pedal neurons have been established (Crow and Tian 2003).In this report we show that Pavlovian conditioning results in light-elicited inhibition of the spike ...

Polysensory Interneuronal Projections to Foot Contractile Pedal Neurons in Hermissenda

“…Results of the present study are consistent with the hypothesis that US-evoked footshortening and US-reduced locomotion emerge independently (Matzel et al 1990). Previous research has identified intrinsic changes with Pavlovian conditioning in two cell types: photoreceptors and type I interneurons (Crow and Alkon 1980;Crow and Tian 2003b;Farley et al 1990). Neural correlates of Pavlovian conditioning-identified in the neural circuit supporting ciliary locomotion and CS-elicited inhibition of ciliary efferent neuron activity-are now well documented (Crow and Tian 2003b).…”

“…Previous research has identified intrinsic changes with Pavlovian conditioning in two cell types: photoreceptors and type I interneurons (Crow and Alkon 1980;Crow and Tian 2003b;Farley et al 1990). Neural correlates of Pavlovian conditioning-identified in the neural circuit supporting ciliary locomotion and CS-elicited inhibition of ciliary efferent neuron activity-are now well documented (Crow and Tian 2003b). However, modification of the neural circuit responsible for CS-elicited foot-shortening is not documented.…”

One‐Trial In Vitro Conditioning of Hermissenda Regulates Phosphorylation of Ser‐122 of Csp24

“…In Hermissenda , Pavlovian conditioning produces intrinsic enhanced excitability in identified neurons 18–21 . Associated with conditioning‐dependent enhanced excitability is the phosphorylation of the cytoskeletal‐related protein Csp24 22,23 .…”

“…In Hermissenda, Pavlovian conditioning produces intrinsic enhanced excitability in identified neurons. [18][19][20][21] Associated with conditioning-dependent enhanced excitability is the phosphorylation of the cytoskeletal-related protein Csp24. 22,23 Intermediate-term memory formation produced by one-trial in vitro conditioning is dependent on the expression and phosphorylation of Csp24.…”

Extending In Vitro Conditioning inAplysiato Analyze Operant and Classical Processes in the Same Preparation

“…To understand such interacting events, it is necessary to first reduce them to their operant and classical components and then join them again under controlled conditions. Laboratory studies of classical conditioning have successfully interrupted the operant-classical feedback loop such that the behavior of the animal is irrelevant and the two environmental events (the conditioned stimulus, CS, which predicts the unconditioned stimulus, US) can be traced from their sensory afferents to the brain and, finally, to the point where they converge and the learning occurs (e.g., Walters and Byrne 1983;Bao et al 1998;Hawkins et al 1998;Kim et al 1998; Lechner et al 2000a,b;Schafe et al 2001;Medina et al 2002;Paschall and Davis 2002;Ressler et al 2002;Antonov et al 2003;Crow and Tian 2003;Davis et al 2003;Epstein et al 2003;Flynn et al 2003;Mozzachiodi et al 2003;Nader 2003). An analogous convergence point between operant behavior and the unconditioned stimulus (or reinforcer in the operant nomenclature) has recently been described in Aplysia (Nargeot et al 1999a,b;Brembs et al 2002).…”