Behavioral and neural bases of extinction learning in Hermissenda.

Joel S Cavallo,Joseph Farley,Brittany N Hamilton

doi:10.3389/fnbeh.2014.00277

Joel S Cavallo, Joseph Farley + Show 1 more

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https://doi.org/10.3389/fnbeh.2014.00277

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Abstract

Extinction of classical conditioning is thought to produce new learning that masks or interferes with the original memory. However, research in the nudibranch Hermissenda crassicornis (H.c.) has challenged this view, and instead suggested that extinction erased the original associative memory. We have re-examined extinction in H.c. to test whether extinguished associative memories can be detected on the behavioral and cellular levels, and to characterize the temporal variables involved. Associative conditioning using pairings of light (CS) and rotation (US) produced characteristic suppression of H.c. phototactic behavior. A single session of extinction training (repeated light-alone presentations) reversed suppressed behavior back to pre-training levels when administered 15 min after associative conditioning. This effect was abolished if extinction was delayed by 23 h, and yet was recovered using extended extinction training (three consecutive daily extinction sessions). Extinguished phototactic suppression did not spontaneously recover at any retention interval (RI) tested (2-, 24-, 48-, 72-h), or after additional US presentations (no observed reinstatement). Extinction training (single session, 15 min interval) also reversed the pairing-produced increases in light-evoked spike frequencies of Type B photoreceptors, an identified site of associative memory storage that is causally related to phototactic suppression. These results suggest that the behavioral effects of extinction training are not due to temporary suppression of associative memories, but instead represent a reversal of the underlying cellular changes necessary for the expression of learning. In the companion article, we further elucidate mechanisms responsible for extinction-produced reversal of memory-related neural plasticity in Type B photoreceptors.

Highlights

Maladaptive learning is thought to be a major factor that underlies human anxiety disorders, such as phobias and post-traumatic stress disorder (PTSD; Garakani et al, 2006; Parsons and Ressler, 2013), as well as pathological conditions, including drug addiction (O’Brien et al, 1998; Di Chiara, 1999; Gass and Chandler, 2013) and eating disorders (Wardle, 1990; Jansen, 1998)
To establish whether spontaneous recovery of pairing-produced phototactic suppression occurred after extinction, phototactic behavior was measured before associative conditioning and at four retention interval (RI), 2, 24, 48, and 72-h post acquisition training
The results indicated that pairings produced phototactic suppression that was reversed by extinction training back to control levels

Summary

Introduction

Maladaptive learning is thought to be a major factor that underlies human anxiety disorders, such as phobias and post-traumatic stress disorder (PTSD; Garakani et al, 2006; Parsons and Ressler, 2013), as well as pathological conditions, including drug addiction (O’Brien et al, 1998; Di Chiara, 1999; Gass and Chandler, 2013) and eating disorders (Wardle, 1990; Jansen, 1998). This contention is supported by recent evidence showing that modified extinction protocols can apparently permanently abolish associative learning In these studies, extinction training delivered shortly after an isolated CS reactivates the original associative memory and is believed to initiate reconsolidation processes that update the original memory with new information (i.e., the CS does not signal the US; Monfils et al, 2009; Schiller et al, 2010). This technique appears to eliminate the behavioral changes produced by associative fear conditioning in rodents (Monfils et al, 2009; Rao-Ruiz et al, 2011; Flavell et al, 2011, but see Chan et al, 2010; Ishii et al, 2012) and humans (Schiller et al, 2010; Steinfurth et al, 2014, but see Golkar et al, 2012; Kindt and Soeter, 2013), and reverses some of the underlying cellular changes associated with fear conditioning (e.g., AMPA GluR1 receptor insertion)

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