The Role of Muscarinic and Nicotinic Cholinergic Neurotransmission in Aversive Conditioning: Comparing Pavlovian Fear Conditioning and Inhibitory Avoidance

Tinsley, Matthew R.; Quinn, Jennifer J.; Fanselow, Michael S.

doi:10.1101/lm.70204

Cited by 87 publications

(68 citation statements)

References 104 publications

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“…Collectively, these results indicate that the cholinergic projections into the BLA facilitate learning of an aversive inhibitory avoidance task (Power and McGaugh 2002;Tinsley et al 2004). Similarly, contextual fear conditioning memories were increased by muscarinic receptor agonism (Cangioli et al 2002) and impaired by muscarinic receptor antagonism (Passani et al 2001;Tinsley et al 2004) in the BLA. Furthermore, an M1 receptor knockout mouse showed deficits in auditory fear learning (Miyakawa et al 2001;Tinsley et al 2004).…”

Section: Basal Forebrain Projection To the Blamentioning

confidence: 68%

“…Conversely, lesions of the NB, thought to have a disproportionately larger effect on BLA cholinergic inputs relative to inputs to other brain areas, impaired the acquisition and consolidation of inhibitory avoidance, an effect that was attenuated by infusion of muscarinic receptor agonists in the BLA (Power and McGaugh 2002;Tinsley et al 2004). Collectively, these results indicate that the cholinergic projections into the BLA facilitate learning of an aversive inhibitory avoidance task (Power and McGaugh 2002;Tinsley et al 2004). Similarly, contextual fear conditioning memories were increased by muscarinic receptor agonism (Cangioli et al 2002) and impaired by muscarinic receptor antagonism (Passani et al 2001;Tinsley et al 2004) in the BLA.…”

Section: Basal Forebrain Projection To the Blamentioning

confidence: 99%

“…Pharmacological agonism of these receptors immediately after training on an inhibitory avoidance task improved task performance (Power et al 2003;Tinsley et al 2004). Conversely, lesions of the NB, thought to have a disproportionately larger effect on BLA cholinergic inputs relative to inputs to other brain areas, impaired the acquisition and consolidation of inhibitory avoidance, an effect that was attenuated by infusion of muscarinic receptor agonists in the BLA (Power and McGaugh 2002;Tinsley et al 2004). Collectively, these results indicate that the cholinergic projections into the BLA facilitate learning of an aversive inhibitory avoidance task (Power and McGaugh 2002;Tinsley et al 2004).…”

Section: Basal Forebrain Projection To the Blamentioning

confidence: 99%

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Input-specific contributions to valence processing in the amygdala

Correia

Goosens

2016

Learn. Mem.

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Reward and punishment are often thought of as opposing processes: rewards and the environmental cues that predict them elicit approach and consummatory behaviors, while punishments drive aversion and avoidance behaviors. This framework suggests that there may be segregated brain circuits for these valenced behaviors. The basolateral amygdala (BLA) is one brain region that contributes to both types of motivated behavior. Individual neurons in the BLA can favor positive over negative valence, or vice versa, but these neurons are intermingled, showing no anatomical segregation. The amygdala receives inputs from many brain areas and current theories posit that encoding of positive versus negative valence by BLA neurons is determined by the wiring of each neuron. Specifically, many projections from other brain areas that respond to positive and negative valence stimuli and predictive cues project strongly to the BLA and likely contribute to valence processing within the BLA. Here we review three of these areas, the basal forebrain, the dorsal raphe nucleus and the ventral tegmental area, and discuss how these may promote encoding of positive and negative valence within the BLA.The basic desire to seek reward and avoid punishment shapes virtually all of behavior, and the ability to discriminate between "good" and "bad" environmental cues is critical for guiding choices and maximizing survival. Thus, understanding the brain circuits that encode motivated behaviors is important because it contributes to our knowledge of how we learn, and it is also essential for understanding human disorders associated with abnormal processing of reward and danger (i.e., emotional disorders), such as anxiety, depression, addiction, and post-traumatic stress disorder (PTSD).The amygdala is one brain area implicated in motivated behaviors and the basolateral complex of the amygdala (BLA) receives information about diverse environmental stimuli from many brain regions. The BLA is thought to encode the association of predictive stimuli with both aversive and appetitive outcomes (Morrison and Salzman 2010;Barberini et al. 2012). Reward and punishment are reinforcers of opposite valence (positive versus negative), and these reinforcers typically lead to opposing behaviors (approach versus avoidance). Many theories have suggested that appetitive and aversive systems act in opponent fashion (Solomon and Corbit 1974;Daw et al. 2002). However, it is unclear how the BLA contributes to this. We do not yet understand the extent to which aversive and appetitive information is processed in parallel BLA circuits, or whether individual BLA neurons are involved in the regulation of both types of motivated behaviors.In this review, we propose several models by which functional segregation of valence can be achieved in the BLA. These models are based on studies describing how BLA neurons respond to reward and aversive stimuli. We then consider whether three major inputs, known to carry valenced information, support or conflict these models, and also discus...

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Section: Basal Forebrain Projection To the Blamentioning

confidence: 68%

Section: Basal Forebrain Projection To the Blamentioning

confidence: 99%

Section: Basal Forebrain Projection To the Blamentioning

confidence: 99%

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Input-specific contributions to valence processing in the amygdala

Correia

Goosens

2016

Learn. Mem.

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“…Memory reconsolidation is frequently studied using Pavlovian fear conditioning (23). The results discussed here were obtained using an inhibitory ("passive or inactive") avoidance response (IAR).…”

Section: Memory Consolidation and Reconsolidation: Methodological Issuesmentioning

confidence: 99%

“…It is clear that the training procedures for these two behavioral paradigms have much in common. However, there are also important differences between fear conditioning and inhibitory avoidance procedures, which may have effects on the neural substrates involved, and may be crucial factors in determining how several pharmacological post-retrieval treatments affect memory reconsolidation (23).…”

Section: Memory Consolidation and Reconsolidation: Methodological Issuesmentioning

confidence: 99%

Pharmacological effects and behavioral interventions on memory consolidation and reconsolidation

Baratti

Boccia

Blake

2009

Braz J Med Biol Res

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In this article, we will review some behavioral, pharmacological and neurochemical studies from our laboratory on mice, which might contribute to our understanding of the complex processes of memory consolidation and reconsolidation. We discuss the post-training (memory consolidation) and post-reactivation (memory reconsolidation) effects of icv infusions of hemicholinium, a central inhibitor of acetylcholine synthesis, of intraperitoneal administration of L-NAME, a non-specific inhibitor of nitric oxide synthase, of intrahippocampal injections of an inhibitor of the transcription factor NF-κB, and the exposure of mice to a new learning situation on retention performance of an inhibitory avoidance response. All treatments impair long-term memory consolidation and retrieval-induced memory processes different from extinction, probably in accordance with the "reconsolidation hypothesis".

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Cannabinoids modulate hippocampal memory and plasticity

2009

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Considerable evidence demonstrates that cannabinoid agonists impair whereas cannabinoid antagonists improve memory and plasticity. However, recent studies suggest that the effects of cannabinoids on learning do not necessarily follow these simple patterns, particularly when emotional memory processes are involved. We investigated the involvement of the cannabinoid system in hippocampal learning and plasticity using the fear-related inhibitory avoidance (IA) and the non-fear-related spatial learning paradigms, and cellular models of learning and memory, i.e., long-term potentiation (LTP) and long-term depression (LTD). We found that microinjection into the CA1 of the CB1/CB2 receptor agonist WIN55,212-2 (5 μg/side) and an inhibitor of endocannabinoid reuptake and breakdown AM404 (200 ng/side) facilitated the extinction of IA, while the CB1 receptor antagonist AM251 (6 ng/side) impaired it. WIN55,212-2 and AM251 did not affect IA conditioning, while AM404 enhanced it, probably due to a drug-induced increase in pain sensitivity. However, in the water maze, systemic or local CA1 injections of AM251, WIN55,212-2, and AM404 all impaired spatial learning. We also found that i.p. administration of WIN55,212-2 (0.5 mg/kg), AM404 (10 mg/kg), and AM251 (2 mg/kg) impaired LTP in the Schaffer collateral-CA1 projection, whereas AM404 facilitated LTD. Our findings suggest diverse effects of the cannabinoid system on CA1 memory and plasticity that cannot be categorized simply into an impairing or an enhancing effect of cannabinoid activation and deactivation, respectively. Moreover, they provide preclinical support for the suggestion that targeting the endocannabinoid system may aid in the treatment of disorders associated with impaired extinction-like processes, such as post-traumatic stress disorder.

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The Role of Muscarinic and Nicotinic Cholinergic Neurotransmission in Aversive Conditioning: Comparing Pavlovian Fear Conditioning and Inhibitory Avoidance

Cited by 87 publications

References 104 publications

Input-specific contributions to valence processing in the amygdala

Input-specific contributions to valence processing in the amygdala

Pharmacological effects and behavioral interventions on memory consolidation and reconsolidation

Cannabinoids modulate hippocampal memory and plasticity

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