Social Memory and the Role of the Hippocampal CA2 Region

Tzakis, Nikolaos; Holahan, Matthew R.

doi:10.3389/fnbeh.2019.00233

Cited by 85 publications

(69 citation statements)

References 101 publications

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“…Using an optogenetic approach, Raam et al ( 2017 ) identified in the hippocampus an output from anterior CA2/CA3 regions to posterior CA1 as the pathway of social stimuli discrimination. These results are consistent with the recognized role of the hippocampus on social cognition regulation (Alexander et al, 2016 ; Okuyama et al, 2016 ; Danjo et al, 2018 ; Phillips et al, 2019 ; Tzakis and Holahan, 2019 ). This regulation is highly associated with the hippocampal posterior CA1 region projection to the prefrontal cortex, hypothalamus, and amygdala, key parts of the emotional reactivity and SDN (Hitti and Siegelbaum, 2014 ; Okuyama et al, 2016 ; Smith et al, 2016 ).…”

Section: Discussionsupporting

confidence: 89%

Increased Endocannabinoid Signaling Reduces Social Motivation in Intact Rats and Does Not Affect Animals Submitted to Early-Life Seizures

Ribeiro

Serro-Azul

Lorena

et al. 2020

Front. Behav. Neurosci.

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The early life status epilepticus (SE) causes high anxiety and chronic socialization abnormalities, revealed by a low preference for social novelty and deficit in social discrimination. This study investigated the involvement of the endocannabinoid system on the sociability in this model, due to its role in social motivation regulation. Male Wistar rats at postnatal day 9 were subjected to pilocarpine-induced neonatal SE and controls received saline. From P60 the groups received vehicle or JZL195 2 h before each behavioral test to increase endocannabinoids availability. In the sociability test, animals subjected to neonatal SE exhibited impaired sociability, characterized by social discrimination deficit, which was unaffected by the JZL195 treatment. In contrast, JZL195-treated control rats showed low sociability and impaired social discrimination. The negative impact of JZL195 over the sociability in control rats and the lack of effect in animals subjected to neonatal SE was confirmed in the social memory paradigm. In this paradigm, as expected for vehicle-treated control rats, the investigation toward the same social stimulus decreased with the sequential exposition and increased toward a novel stimulus. In animals subjected to neonatal SE, regardless of the treatment, as well as in JZL195-treated control rats, the investigation toward the same social stimulus was significantly reduced with no improvement toward a novel stimulus. Concerning the locomotion, the JZL195 increased it only in control rats. After behavioral tests, brain tissues of untreated animals were used for CB1 receptor quantification by Elisa and for gene expression by RT-PCR: no difference between control and experimental animals was noticed. The results reinforce the evidence that the early SE causes chronic socialization abnormalities, revealed by the low social interest for novelty and impaired social discrimination. The dual FAAH/MAGL inhibitor (JZL195) administration before the social encounter impaired the social interaction in intact rats with no effect in animals subjected to early-life seizures.

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Section: Discussionsupporting

confidence: 89%

Increased Endocannabinoid Signaling Reduces Social Motivation in Intact Rats and Does Not Affect Animals Submitted to Early-Life Seizures

Ribeiro

Serro-Azul

Lorena

et al. 2020

Front. Behav. Neurosci.

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“…Using MRI analysis, we found no major structural alterations in the brain of our mutants except larger olfactory bulbs and a smaller hippocampus. Our data are in agreement with studies showing that the hippocampus plays a critical role in social memory and recognition (Kogan et al, 2000;Maaswinkel et al, 1996;Okuyama, 2018;Raam et al, 2017;Tzakis and Holahan, 2019). It is possible that social memories also rely on different subregions of the hippocampus, different networks and connections and/or different molecular pathways.…”

Section: A Central Role Of the Hippocampus In Scrib Dependent Social supporting

confidence: 92%

Scribble controls social behaviors through the regulation of the ERK/Mnk1 pathway

Moreau

Pietropaolo

Ezan

et al. 2020

Preprint

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Social behavior is a basic domain affected in several neurodevelopmental disorders. Indeed, deficits in social interest, interactions and recognition represent core symptoms of Autism Spectrum Disorder but are also found associated with a heterogeneous set of neuropsychiatric and rare disorders. The SCRIB gene that codes for the polarity protein SCRIBBLE has been identified as a risk gene for spina bifida, the most common type of open neural tube defect, found at high frequencies in autistic patients, as other congenital anomalies, while the deletions/mutations of the 8q24.3 region encompassing SCRIB genes is associated with multisyndromic and rare disorders. Nonetheless, the potential link between SCRIB and ASD-relevant social phenotypes has not been investigated yet. Hence, we performed an extensive behavioral characterization of the circletail line that carries a mutated version of Scrib. Scribcrc/+ mice displayed reduced social interest, lack of preference for social novelty and social reward, and reduced social habituation while other behavioral domains were unaltered. Social deficits were associated with reduced hippocampal volume, upregulation of ERK phosphorylation in specific hippocampal regions, together with increased c-Fos activity in the same brain areas. Importantly, the social alterations were rescued by both direct and indirect pERK inhibition. These results support a specific link between polarity genes, social behaviors and hippocampal functionality, thus suggesting a role for SCRIB in the etiopathology of neurodevelopmental disorders. Furthermore, our data demonstrate the crucial role of the MAPK/ERK signaling pathway, in underlying the social deficits induced by SCRIB mutation, thus supporting its relevance as a therapeutic target.

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“…Overall, delayed maturation of PNNs in the CA1 might be responsible for long-lasting cognitive/psychiatric impairments. The hippocampal area CA2 is required for the formation of social memories, and particularly social recognition memory, namely the ability to recognize a novel or familiar conspecific [ 118 ]. The CA2 contains a population of large pyramidal neurons [ 119 ], which are surrounded by prominent PNNs.…”

Section: Pnns and Brain Maturationmentioning

confidence: 99%

An Extracellular Perspective on CNS Maturation: Perineuronal Nets and the Control of Plasticity

Carulli

Verhaagen

2021

IJMS

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During restricted time windows of postnatal life, called critical periods, neural circuits are highly plastic and are shaped by environmental stimuli. In several mammalian brain areas, from the cerebral cortex to the hippocampus and amygdala, the closure of the critical period is dependent on the formation of perineuronal nets. Perineuronal nets are a condensed form of an extracellular matrix, which surrounds the soma and proximal dendrites of subsets of neurons, enwrapping synaptic terminals. Experimentally disrupting perineuronal nets in adult animals induces the reactivation of critical period plasticity, pointing to a role of the perineuronal net as a molecular brake on plasticity as the critical period closes. Interestingly, in the adult brain, the expression of perineuronal nets is remarkably dynamic, changing its plasticity-associated conditions, including memory processes. In this review, we aimed to address how perineuronal nets contribute to the maturation of brain circuits and the regulation of adult brain plasticity and memory processes in physiological and pathological conditions.

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Social Memory and the Role of the Hippocampal CA2 Region

Cited by 85 publications

References 101 publications

Increased Endocannabinoid Signaling Reduces Social Motivation in Intact Rats and Does Not Affect Animals Submitted to Early-Life Seizures

Increased Endocannabinoid Signaling Reduces Social Motivation in Intact Rats and Does Not Affect Animals Submitted to Early-Life Seizures

Scribble controls social behaviors through the regulation of the ERK/Mnk1 pathway

An Extracellular Perspective on CNS Maturation: Perineuronal Nets and the Control of Plasticity

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