Modulation of the storage of social recognition memory by neurotransmitter systems in the insular cortex

Cavalcante, Lorena Evelyn Silva; Zinn, Carolina Garrido; Schmidt, Scheila Daiane; Saenger, Bruna Freitas; Ferreira, Flávia Fagundes; Furini, Cristiane Regina Guerino; Myskiw, Jociane C.; Izquierdo, Iván

doi:10.1016/j.bbr.2017.07.044

Cited by 35 publications

(16 citation statements)

References 37 publications

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“…We previously reported that inactivation of the pIC increased the latency to express gastric malaise and disrupted drug craving (Contreras et al, 2007) and that the anterior insula is involved in context/drug effect association (Contreras et al, 2012) as well as in consolidation of auditory fear memory (Casanova et al, 2016). The involvement of the IC in threat memory is also consistent with investigations showing that the IC plays an important role in taste memory formation (Bermúdez-Rattoni et al, 2004), object recognition memory (Bermudez-Rattoni et al, 2005), and social memory (Cavalcante et al, 2017). However, another limitation of the present study is that we cannot rule out the possibility that context pre-exposure before the first cat odor test could have decreased associative strength between cat odor and context cues (i.e., latent inhibition) which may have contributed to our findings.…”

Section: Discussionsupporting

confidence: 76%

Interoceptive Insular Cortex Mediates Both Innate Fear and Contextual Threat Conditioning to Predator Odor

Rodríguez

Cerić

Murgas

et al. 2020

Front. Behav. Neurosci.

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The insular cortex (IC), among other brain regions, becomes active when humans experience fear or anxiety. However, few experimental studies in rats have implicated the IC in threat responses. We have recently reported that inactivation of the primary interoceptive cortex (pIC) during pre-training, or the intra-pIC blockade of protein synthesis immediately after training, impaired the consolidation of auditory fear conditioning. The present study was designed to investigate the role of the pIC in innate and learned defensive responses to predator odor. Freezing behavior was elicited by single or repetitive exposures to a collar that had been worn by a domestic cat. Sessions were video-recorded and later scored by video observation. We found that muscimol inactivation of the pIC reduced the expression of freezing reaction in response to a single or repeated exposure to cat odor. We also found that pIC inactivation with muscimol impaired conditioning of fear to the context in which rats were exposed to cat odor. Furthermore, neosaxitoxin inactivation of the pIC resulted in a prolonged and robust reduction in freezing response in subsequent re-exposures to cat odor. In addition, freezing behavior significantly correlated with the neural activity of the IC. The present results suggest that the IC is involved in the expression of both innate and learned fear responses to predator odor.

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Section: Discussionsupporting

confidence: 76%

Interoceptive Insular Cortex Mediates Both Innate Fear and Contextual Threat Conditioning to Predator Odor

Rodríguez

Cerić

Murgas

et al. 2020

Front. Behav. Neurosci.

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“…Systemic and direct infusion of DA D1 receptor agonists either into the frontal cortex or into the nucleus accumbens improved short-term SRM in rats (Di Cara et al, 2007). Intra-insular cortex administration of agonists for DA D1/D5 receptors, β-adrenergic and serotonergic 5-HT 1A receptors improved the consolidation of SRM in rats (Cavalcante et al, 2017). Further, the potentiation of CA3-CA1 hippocampal synapses facilitates the consolidation of object recognition memory (Clarke et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

“…Different lines of investigation suggested a contribution of the dopaminergic system in distinct brain regions beyond the nucleus accumbens to the generation of short-term and long-term SRM of laboratory rats. Among them, the hippocampus and striatum are likely to be interesting brain areas (Garrido Zinn et al, 2016; Cavalcante et al, 2017) in which an increased DA signaling might contribute to a “stabilization” of the “SRM trace” and thereby making it resistant against interference.…”

Section: Discussionmentioning

confidence: 99%

Differential Effects of Novel Dopamine Reuptake Inhibitors on Interference With Long-Term Social Memory in Mice

Camats-Perna

Kalaba

Ebner

et al. 2019

Front. Behav. Neurosci.

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In the laboratory, long-term social recognition memory (SRM) in mice is highly susceptible to proactive and retroactive interference. Here, we investigate the ability of novel designed dopamine (DA) re-uptake inhibitors ( rac -CE-123 and S -CE-123) to block retroactive and proactive interference, respectively. Our data show that administration of rac -CE-123 30 min before learning blocks retroactive interference that has been experimentally induced at 3 h, but not at 6 h, post-learning. In contrast, S-CE-123 treatment 30 min before learning blocked the induction of retroactive interference at 6 h, but not 3 h, post-learning. Administration of S -CE-123 failed to interfere with proactive interference at both 3 h and 6 h. Analysis of additional behavioral parameters collected during the memory task implies that the effects of the new DA re-uptake inhibitors on retroactive and proactive interference cannot easily be explained by non-specific effects on the animals’ general social behavior. Furthermore, we assessed the mechanisms of action of drugs using intracerebral in vivo -microdialysis technique. The results revealed that administration of rac -CE-123 and S -CE-123 dose-dependently increased DA release within the nucleus accumbens of freely behaving mice. Thus, the data from the present study suggests that the DA re-uptake inhibitors tested protect the consolidation of long-term social memory against interference for defined durations after learning. In addition, the data implies that DA signaling in distinct brain areas including the nucleus accumbens is involved in the consolidation of SRM in laboratory mice.

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“…Catecholamines individually and complementarily modulate cortical functions (Chandler, Waterhouse, & Gao, ). As recently shown for several learning tasks involving hippocampal and cortical brain regions, dopamine signalling by D 1/5 ‐receptors and noradrenaline signalling by β‐receptors may independently modulate memory consolidation (Cavalcante et al., ; Moncada, ; Moncada et al., ; Ouyang, Young, Lestini, Schutsky, & Thomas, ). Based on these considerations, we hypothesised a functional importance also of β‐adrenergic signalling in the auditory cortex for auditory discrimination learning and memory.…”

Section: Introductionmentioning

confidence: 74%

β‐adrenergic modulation of discrimination learning and memory in the auditory cortex

Schicknick

Henschke

Budinger

et al. 2019

Eur J of Neuroscience

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Despite vast literature on catecholaminergic neuromodulation of auditory cortex functioning in general, knowledge about its role for long‐term memory formation is scarce. Our previous pharmacological studies on cortex‐dependent frequency‐modulated tone‐sweep discrimination learning of Mongolian gerbils showed that auditory‐cortical D1/5‐dopamine receptor activity facilitates memory consolidation and anterograde memory formation. Considering overlapping functions of D1/5‐dopamine receptors and β‐adrenoceptors, we hypothesised a role of β‐adrenergic signalling in the auditory cortex for sweep discrimination learning and memory. Supporting this hypothesis, the β1/2‐adrenoceptor antagonist propranolol bilaterally applied to the gerbil auditory cortex after task acquisition prevented the discrimination increment that was normally monitored 1 day later. The increment in the total number of hurdle crossings performed in response to the sweeps per se was normal. Propranolol infusion after the seventh training session suppressed the previously established sweep discrimination. The suppressive effect required antagonist injection in a narrow post‐session time window. When applied to the auditory cortex 1 day before initial conditioning, β1‐adrenoceptor‐antagonising and β1‐adrenoceptor‐stimulating agents retarded and facilitated, respectively, sweep discrimination learning, whereas β2‐selective drugs were ineffective. In contrast, single‐sweep detection learning was normal after propranolol infusion. By immunohistochemistry, β1‐ and β2‐adrenoceptors were identified on the neuropil and somata of pyramidal and non‐pyramidal neurons of the gerbil auditory cortex. The present findings suggest that β‐adrenergic signalling in the auditory cortex has task‐related importance for discrimination learning of complex sounds: as previously shown for D1/5‐dopamine receptor signalling, β‐adrenoceptor activity supports long‐term memory consolidation and reconsolidation; additionally, tonic input through β1‐adrenoceptors may control mechanisms permissive for memory acquisition.

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Modulation of the storage of social recognition memory by neurotransmitter systems in the insular cortex

Cited by 35 publications

References 37 publications

Interoceptive Insular Cortex Mediates Both Innate Fear and Contextual Threat Conditioning to Predator Odor

Interoceptive Insular Cortex Mediates Both Innate Fear and Contextual Threat Conditioning to Predator Odor

Differential Effects of Novel Dopamine Reuptake Inhibitors on Interference With Long-Term Social Memory in Mice

β‐adrenergic modulation of discrimination learning and memory in the auditory cortex

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