Abstract:In reconsolidation studies, memories are typically retrieved by an exposure to a single conditioned stimulus (CS). We have previously demonstrated that reconsolidation processes are CS-selective, suggesting that memories retrieved by the CS exposure are discrete and reconsolidate separately. Here, using a compound stimulus in which two distinct CSs are concomitantly paired with the same aversive unconditioned stimulus (US), we show in rats that reexposure to one of the components of the compound CS triggers ex… Show more
“…First, it is important to note that reactivation of the appetitive memory through re-exposure to just the auditory element of the compound stimulus must have destabilised the entire compound CS-sucrose association, as discriminated approach to the visual component was impaired. This is consistent with findings from a study on fear memory reconsolidation, in which intra-amygdala anisomycin following reactivation through re-exposure to the visual component resulted in subsequent impaired conditioned freezing to the auditory component (Debiec et al 2013). However, the study by Debiec et al (2013) did not test conditioned freezing to the full compound stimulus.…”
Section: Discussionsupporting
confidence: 90%
“…Sign-tracking paradigms in rodents traditionally use simple visual stimuli alone (Bussey et al 1997), and reconsolidation deficits have been observed in such settings (Lee and Everitt 2008b; Cogan et al 2019). However, while more translationally-relevant compound stimuli have been studied in fear memory reconsolidation studies, showing that re-exposure to one component triggers reconsolidation of the other element (Debiec et al 2013), it remains unclear whether such principles of memory destabilization also apply in appetitive settings.…”
Studies of memory reconsolidation of pavlovian memories have typically employed unimodal conditioned stimuli, despite the use of multimodal compound stimuli in other settings. Here we studied sign-tracking behaviour to a compound audiovisual stimulus. First, we observed not unexpectedly that sign-tracking was poorer to the audiovisual compound than to unimodal visual stimuli. Then, we showed that, depending on the parameters of compound stimulus re-exposure at memory reactivation, systemic MK-801 treatment either impaired extinction to improve signtracking at test, or disrupted reconsolidation to impair test behaviour. When memory reactivation consisted of re-exposure to only the auditory component of the compound stimulus, we observed sign-tracking impairments following MK-801 treatment, but only under certain test conditions. This was in contrast to the consistent impairment following reactivation with the full audiovisual compound. Moreover, the parameters of auditory stimulus presentation to enable MK-801-induced impairment at test varied depending on whether the stimulus was presented within or outside the training context. These findings suggest that behaviour under the control of appetitive pavlovian compound stimuli can be modulated by targeting both extinction and reconsolidation, and that it is not necessary to re-expose to the full compound stimulus in order to achieve a degree of modulation of behaviour.
“…First, it is important to note that reactivation of the appetitive memory through re-exposure to just the auditory element of the compound stimulus must have destabilised the entire compound CS-sucrose association, as discriminated approach to the visual component was impaired. This is consistent with findings from a study on fear memory reconsolidation, in which intra-amygdala anisomycin following reactivation through re-exposure to the visual component resulted in subsequent impaired conditioned freezing to the auditory component (Debiec et al 2013). However, the study by Debiec et al (2013) did not test conditioned freezing to the full compound stimulus.…”
Section: Discussionsupporting
confidence: 90%
“…Sign-tracking paradigms in rodents traditionally use simple visual stimuli alone (Bussey et al 1997), and reconsolidation deficits have been observed in such settings (Lee and Everitt 2008b; Cogan et al 2019). However, while more translationally-relevant compound stimuli have been studied in fear memory reconsolidation studies, showing that re-exposure to one component triggers reconsolidation of the other element (Debiec et al 2013), it remains unclear whether such principles of memory destabilization also apply in appetitive settings.…”
Studies of memory reconsolidation of pavlovian memories have typically employed unimodal conditioned stimuli, despite the use of multimodal compound stimuli in other settings. Here we studied sign-tracking behaviour to a compound audiovisual stimulus. First, we observed not unexpectedly that sign-tracking was poorer to the audiovisual compound than to unimodal visual stimuli. Then, we showed that, depending on the parameters of compound stimulus re-exposure at memory reactivation, systemic MK-801 treatment either impaired extinction to improve signtracking at test, or disrupted reconsolidation to impair test behaviour. When memory reactivation consisted of re-exposure to only the auditory component of the compound stimulus, we observed sign-tracking impairments following MK-801 treatment, but only under certain test conditions. This was in contrast to the consistent impairment following reactivation with the full audiovisual compound. Moreover, the parameters of auditory stimulus presentation to enable MK-801-induced impairment at test varied depending on whether the stimulus was presented within or outside the training context. These findings suggest that behaviour under the control of appetitive pavlovian compound stimuli can be modulated by targeting both extinction and reconsolidation, and that it is not necessary to re-expose to the full compound stimulus in order to achieve a degree of modulation of behaviour.
“…This finding is explained by observing that in our model learning only affects the CSs associated with the current inferred latent cause. In a recent study, Debiec et al (2013) showed that cue-specificity of reconsolidation depends on separately training the two CSs; when they are trained in compound, reactivating one CS can render the other CS labile. Our model reproduces this effect (Figure 7B) as in this case the compound cue is assigned to a single latent cause that generates both CSs and the US, thereby coupling the two CSs.10.7554/eLife.23763.009Figure 7.Cue-specificity of amnestic treatment.( A ) Disruption of memory modification by amnestic treatment affects the reactivated cue (CSr) but not the non-reactivated cue (CSn).…”
Retrieving a memory can modify its influence on subsequent behavior. We develop a computational theory of memory modification, according to which modification of a memory trace occurs through classical associative learning, but which memory trace is eligible for modification depends on a structure learning mechanism that discovers the units of association by segmenting the stream of experience into statistically distinct clusters (latent causes). New memories are formed when the structure learning mechanism infers that a new latent cause underlies current sensory observations. By the same token, old memories are modified when old and new sensory observations are inferred to have been generated by the same latent cause. We derive this framework from probabilistic principles, and present a computational implementation. Simulations demonstrate that our model can reproduce the major experimental findings from studies of memory modification in the Pavlovian conditioning literature.DOI:
http://dx.doi.org/10.7554/eLife.23763.001
“…During the periweaning period, the development of the hippocampus allows the processing and encoding of more complex configurations of stimuli which make the learning context (Debiec et al, 2013; Pearce & Bouton, 2001; Fanselow, 2000), and by PN 24 contextual threat conditioning emerges (Raineki et al, 2010; Rudy, 1993) (Fig. 4).…”
Section: Development Of Associative Threat Learningmentioning
What an animal needs to learn to survive is altered dramatically as they change from dependence on the parent for protection to independence and reliance on self-defense. This transition occurs in most altricial animals, but our understanding of the behavioral neurobiology has mostly relied on the infant rat. The transformation from dependence to independence occurs over three weeks in pups and is accompanied by complex changes in responses to both natural and learned threats and the supporting neural circuitry. Overall, in early life, the threat system is quiescent and learning is biased towards acquiring attachment related behaviors to support attachment to the caregiver and proximity seeking. Caregiver-associated cues learned in infancy have the ability to provide a sense of safety throughout lifetime. This attachment/safety system is activated by learning involving presumably pleasurable stimuli (food, warmth) but also painful stimuli (tailpinch, moderate shock). At about the midway point to independence, pups begin to have access to the adult-like amygdala-dependent threat system and amygdala-dependent responses to natural dangers such as predator odors. However, pups have the ability to switch between the infant and adult-like system, which is controlled by maternal presence and modification of stress hormones. Specifically, if the pup is alone, it will learn fear but if with the mother it will learn attachment (10–15 days of age). As pups begin to approach weaning, pups lose access to the attachment system and rely only on the amygdala-dependent threat system. However, pups learning system is complex and exhibits flexibility that enables the mother to override the control of the attachment circuit, since newborn pups may acquire threat responses from the mother expressing fear in their presence. Together, these data suggest that the development of pups’ threat learning system is not only dependent upon maturation of the amygdala, but it is also exquisitely controlled by the environment. Most notably the mother can switch pup learning between attachment to threat learning in a moment’s notice. This enables the mother to navigate pup’s learning about the world and what is threatening and what is safe.
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