‘Pain relief’ learning in fruit flies

Yarali, Ayse; Niewalda, Thomas; Chen, Yi chun; Tanimoto, Hiromu; Duerrnagel, Stefan; Gerber, Bertram

doi:10.1016/j.anbehav.2008.05.025

Cited by 56 publications

(90 citation statements)

References 27 publications

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“…We noted that, in flies at least, memories after fear conditioning are temporally less stable than memories after relief conditioning (see Fig. 7 in Yarali et al 2008); if this were the case in humans too, the consequences of degraded relief learning may surface with delay, consistent with the incubation often observed for PTSD symptoms (Bonne et al 2004). In any event, our results prompt us to consider the role of relief conditioning in the development and maintenance of exaggerated risk taking, excessive safety seeking, posttraumatic stress, and panic disorders, including the question of whether the chosen therapy is differentially effective for fear and relief memories, or not.…”

Section: Discussionmentioning

confidence: 99%

“…2B, 4) and in humans (Andreatta et al 2010; for related results in flies, see Tanimoto et al 2004;Yarali et al 2008). Importantly, such conditioned relief recruits and depends on the striatum, particularly its ventral part (Figs.…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, humans explicitly report a negative valence in both cases, despite the opponency of the implicit valences (Andreatta et al 2010). Notably, this human paradigm, similar to the fly paradigm (Tanimoto et al 2004;Yarali et al 2008), enables assaying conditioned fear and conditioned relief directly and within the same behavioral setting. We reasoned that conditioned relief crucially depends on striatal networks, on the one hand because lesion studies in animals revealed that the attenuation of startle responses due to positively valenced events depends on striatal circuits (Koch et al 1996), and on the other hand because human fMRI studies found evidence that the reduction (Seymour et al 2005), the omission (Leknes et al 2011), or the termination (Becerra and Borsook 2008) of an expected painful stimulation is associated with activity in the ventral striatum.…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

“…In Drosophila, such training establishes conditioned approach to the stimulus (Tanimoto et al 2004;Yarali et al 2008), indicating that it has been learned as a signal for "relief" from shock (Solomon 1980;Wagner 1981) or for "respite" (Lohr et al 2007) or "safety" (Sutton and Barto 1990;Chang et al 2003;Leknes et al 2011) related to the shock-free safe period within the shock-associated dangerous experimental context. The relief-based explanation appears more fitting in this case, because "safety conditioning" should rely on the strength of the context-shock association (e.g., Chang et al 2003) and on the length of the shock-free safe period following the stimulus (e.g., Moscovitch and LoLordo 1968), but neither of these seems to be the case in Drosophila (Yarali et al 2008).…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

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Onset and offset of aversive events establish distinct memories requiring fear and reward networks

et al. 2012

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Two things are worth remembering about an aversive event: What made it happen? What made it cease? If a stimulus precedes an aversive event, it becomes a signal for threat and will later elicit behavior indicating conditioned fear. However, if the stimulus is presented upon cessation of the aversive event, it elicits behavior indicating conditioned "relief." What are the neuronal bases for such learning? Using functional magnetic resonance imaging (fMRI) in humans we found that a fearconditioned stimulus activates amygdala but not striatum, whereas a relief-conditioned stimulus activates striatum but not amygdala. Correspondingly, acute inactivation of amygdala or of ventral striatum in rats respectively abolished only conditioned fear or only conditioned relief. Thus, the behaviorally opponent memories supported by onset and offset of aversive events engage and require fear and reward networks, respectively. This may explain attraction to stimuli associated with the cessation of trauma or of panic attacks. [Supplemental material is available for this article.]We avoid pain and seek reward. To this end, stimuli can become associated with these respective salient events (Pavlov 1927). For example, if a visual stimulus is repeatedly followed by an electric shock, it will be learned as a threat and will elicit conditioned fear. A behavioral indicator of such conditioned fear in humans and other mammals is increased "jumpiness" measured as an increased startle response in the presence of the learned stimulus (Davis et al. 1993;Fendt and Fanselow 1999;Grillon and Baas 2003). The neuronal basis of such conditioned fear and the crucial involvement of the amygdala is well examined in humans and rodents (Davis et

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

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Onset and offset of aversive events establish distinct memories requiring fear and reward networks

et al. 2012

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“…Interestingly, in the fruit fly as well as in vertebrates, it has been suggested that backward conditioning of an aversive US results in a positive response toward the backward conditioned odor (Tanimoto et al 2004;Yarali et al 2008;Andreatta et al 2010Andreatta et al , 2012. This response was termed "relief-learning" (Tanimoto et al 2004).…”

Section: 'Punishment Learning' During Backward Conditioning With a Rementioning

confidence: 99%

Short- and long-term memories formed upon backward conditioning in honeybees (Apis mellifera)

et al. 2014

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In classical conditioning, the temporal sequence of stimulus presentations is critical for the association between the conditioned stimulus (CS) and the unconditioned stimulus (US). In forward conditioning, the CS precedes the US and is learned as a predictor for the US. Thus it acquires properties to elicit a behavioral response, defined as excitatory properties. In backward conditioning, the US precedes the CS. The CS might be learned as a predictor for the cessation of the US acquiring inhibitory properties that inhibit a behavioral response. Interestingly, behavior after backward conditioning is controlled by both excitatory and inhibitory properties of the CS, but the underlying mechanisms determining which of these opposing properties control behavior upon retrieval is poorly understood. We performed conditioning experiments in the honeybee (Apis mellifera) to investigate the CS properties that control behavior at different time points after backward conditioning. The CS properties, as characterized by the retardation or enhancement of subsequent acquisition, were examined 30 min and 24 h after backward conditioning. We found that 30 min after backward conditioning, the CS acquired an inhibitory property during backward conditioning depending on the intertrial interval, the number of trials, and the odor used as the CS. One day after backward conditioning, we observed significant retardation of acquisition. In addition, we demonstrated an enhanced, generalized odor response in the backward conditioned group compared to untreated animals. These results indicate that two long-lasting opposing memories have been formed in parallel: one about the excitatory properties of the CS and one about the inhibitory properties of the CS.

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Invertebrates

Mosley¹,

Lewbart²

2014

Zoo Animal and Wildlife Immobilization and Anesthesia

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‘Pain relief’ learning in fruit flies

Cited by 56 publications

References 27 publications

Onset and offset of aversive events establish distinct memories requiring fear and reward networks

Onset and offset of aversive events establish distinct memories requiring fear and reward networks

Short- and long-term memories formed upon backward conditioning in honeybees (Apis mellifera)

Invertebrates

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