Hippocampal cytogenesis abrogation impairs inter-regional communication between the hippocampus and prefrontal cortex and promotes the time-dependent manifestation of emotional and cognitive deficits

Mateus‐Pinheiro, António; Patrício, Patrícia; Alves, Nuno Dinis; Macedo, Joana Espiga de; Caetano, Inês; Silveira-Rosa, Tiago; Araújo, Bruna; Mateus-Pinheiro, Miguel; Silva‐Correia, Joana; Sardinha, Vanessa Morais; Loureiro‐Campos, Eduardo; Rodrigues, Ana João; Oliveira, João Filipe; Bessa, João M.; Sousa, Nuno; Pinto, Luís

doi:10.1038/s41380-021-01287-8

Cited by 14 publications

(16 citation statements)

References 75 publications

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“…In addition, they control network oscillations (Lacefield et al, 2012;McHugh et al, 2022) most probably via inhibitory interneurons (Drew et al, 2016;Lodge and Bischofberger, 2019;Park et al, 2015;Temprana et al, 2015). By modulating the temporal dynamics of hippocampal network activity they could exert their influence beyond hippocampal activity (Mateus-Pinheiro et al, 2021). In our experiments, we did not find any effect of the chemogenetic stimulation of adult-born neurons on the activity of granular cell layer of the DG.…”

Section: Discussioncontrasting

confidence: 46%

Chemogenetic Stimulation of Adult Neurogenesis, and Not Neonatal Neurogenesis, Is Sufficient to Improve Long-Term Memory Accuracy

Lods,

Mortessagne,

Pacary

et al. 2022

SSRN Journal

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Section: Discussioncontrasting

confidence: 46%

Chemogenetic Stimulation of Adult Neurogenesis, and Not Neonatal Neurogenesis, Is Sufficient to Improve Long-Term Memory Accuracy

Lods,

Mortessagne,

Pacary

et al. 2022

SSRN Journal

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“…This apparent discrepancy may be related to the specific time of AP2γ deletion on these different mice models. Yet, similar electrophysiological deficits in dHIP-mPFC coherence were observed in a rat model of hippocampal cytogenesis abrogation, which also denote long-term manifestation of emotional and cognitive deficits ( Mateus-Pinheiro et al, 2021 ). Moreover, the integrity of the hippocampus-to-PFC circuitry was described to be relevant for the action of antidepressants, such as ketamine ( Carreno et al, 2016 ), which promote neurogenesis, suggesting that AP2γ may be involved in conserving this neuronal circuit.…”

Section: Discussionmentioning

confidence: 78%

Constitutive deficiency of the neurogenic hippocampal modulator AP2γ promotes anxiety-like behavior and cumulative memory deficits in mice from juvenile to adult periods

Loureiro‐Campos

Mateus‐Pinheiro

Patrício

et al. 2021

eLife

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The transcription factor activating protein two gamma (AP2γ) is an important regulator of neurogenesis both during embryonic development as well as in the postnatal brain, but its role for neurophysiology and behavior at distinct postnatal periods is still unclear. In this work, we explored the neurogenic, behavioral, and functional impact of a constitutive and heterozygous AP2γ deletion in mice from early postnatal development until adulthood. AP2γ deficiency promotes downregulation of hippocampal glutamatergic neurogenesis, altering the ontogeny of emotional and memory behaviors associated with hippocampus formation. The impairments induced by AP2γ constitutive deletion since early development leads to an anxious-like phenotype and memory impairments as early as the juvenile phase. These behavioral impairments either persist from the juvenile phase to adulthood or emerge in adult mice with deficits in behavioral flexibility and object location recognition. Collectively, we observed a progressive and cumulative impact of constitutive AP2γ deficiency on the hippocampal glutamatergic neurogenic process, as well as alterations on limbic-cortical connectivity, together with functional behavioral impairments. The results herein presented demonstrate the modulatory role exerted by the AP2γ transcription factor and the relevance of hippocampal neurogenesis in the development of emotional states and memory processes.

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“…As a hypothesis-driven fMRI study, the bilateral amygdala and hippocampus, which are known to be associated with cognition and emotion in well-replicated studies ( Montagne et al, 2019 ; de Carvalho et al, 2021 ; Dogra et al, 2021 ; Duan et al, 2021 ; Mateus-Pinheiro et al, 2021 ; Nguyen et al, 2021 ), were selected as seed regions for subsequent rsFC analyses. Our results indicated that migraineurs showed decreased rsFC mainly in the occipital lobe, such as the bilateral calcarine/cuneus and lingual gyrus, using the left amygdala and left hippocampus as seeds.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies have shown that migraineurs exhibited alterations in the rsFC of amygdala and hippocampus ( Hadjikhani et al, 2013 ; Zhu et al, 2021 ), and the two brain regions were associated with cognition and emotion ( Montagne et al, 2019 ; de Carvalho et al, 2021 ; Dogra et al, 2021 ; Duan et al, 2021 ; Mateus-Pinheiro et al, 2021 ; Nguyen et al, 2021 ). Considering the differences in neuropsychological performance between migraine and TTH ( Waldie et al, 2002 ; Gil-Gouveia et al, 2015 , 2016 ; Huang et al, 2017 ; Puledda et al, 2017 ; Karsan and Goadsby, 2018 ; Vuralli et al, 2018 ), we chose the bilateral amygdala and hippocampus as seed regions for rsFC analyses, to explore the potential rsFC features that may distinguish the two types of headache.…”

Section: Methodsmentioning

confidence: 99%

“…The interaction between neuropsychological performance and neuroimaging features may be one of the potential characteristics to distinguish patients with migraine from patients with TTH. The amygdala and hippocampus are the key brain regions related to cognition and emotion ( Montagne et al, 2019 ; de Carvalho et al, 2021 ; Dogra et al, 2021 ; Duan et al, 2021 ; Mateus-Pinheiro et al, 2021 ; Nguyen et al, 2021 ). The alterations in rsFC of the two brain regions have been reported in migraineurs when compared to healthy controls (HCs) ( Hadjikhani et al, 2013 ; Zhu et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

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Functional Connectivity Features of Resting-State Functional Magnetic Resonance Imaging May Distinguish Migraine From Tension-Type Headache

Wang

et al. 2022

Front. Neurosci.

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BackgroundMigraineurs often exhibited abnormalities in cognition, emotion, and resting-state functional connectivity (rsFC), whereas patients with tension-type headache (TTH) rarely exhibited these abnormalities. The aim of this study is to explore whether rsFC alterations in brain regions related to cognition and emotion could be used to distinguish patients with migraine from patients with TTH.MethodsIn this study, Montreal Cognitive Assessment (MoCA), Self-Rating Anxiety Scale (SAS), Self-Rating Depression Scale (SDS), and rsFC analyses were used to assess the cognition, anxiety, and depression of 24 healthy controls (HCs), 24 migraineurs, and 24 patients with TTH. Due to their important roles in neuropsychological functions, the bilateral amygdala and hippocampus were chosen as seed regions for rsFC analyses. We further assessed the accuracy of the potential rsFC alterations for distinguishing migraineurs from non-migraineurs (including HCs and patients with TTH) by the receiver operating characteristic (ROC) analysis. Associations between headache characteristics and rsFC features were calculated using a multi-linear regression model. This clinical trial protocol has been registered in the Chinese Clinical Trial Registry (registry number: ChiCTR1900024307, Registered: 5 July 2019-Retrospectively registered, http://www.chictr.org.cn/showproj.aspx?proj=40817).ResultsMigraineurs showed lower MoCA scores (p = 0.010) and higher SAS scores (p = 0.017) than HCs. Migraineurs also showed decreased rsFC in the bilateral calcarine/cuneus, lingual gyrus (seed: left amygdala), and bilateral calcarine/cuneus (seed: left hippocampus) in comparison to HCs and patients with TTH. These rsFC features demonstrated significant distinguishing capabilities and got a sensitivity of 82.6% and specificity of 81.8% with an area under the curve (AUC) of 0.868. rsFC alterations showed a significant correlation with headache frequency in migraineurs (p = 0.001, Pc = 0.020).ConclusionThe rsFC of amygdala and hippocampus with occipital lobe can be used to distinguish patients with migraine from patients with TTH.Clinical Trial Registration[http://www.chictr.org.cn/showproj.aspx?proj=40817], identifier [ChiCTR1900024307].

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Hippocampal cytogenesis abrogation impairs inter-regional communication between the hippocampus and prefrontal cortex and promotes the time-dependent manifestation of emotional and cognitive deficits

Cited by 14 publications

References 75 publications

Chemogenetic Stimulation of Adult Neurogenesis, and Not Neonatal Neurogenesis, Is Sufficient to Improve Long-Term Memory Accuracy

Chemogenetic Stimulation of Adult Neurogenesis, and Not Neonatal Neurogenesis, Is Sufficient to Improve Long-Term Memory Accuracy

Constitutive deficiency of the neurogenic hippocampal modulator AP2γ promotes anxiety-like behavior and cumulative memory deficits in mice from juvenile to adult periods

Functional Connectivity Features of Resting-State Functional Magnetic Resonance Imaging May Distinguish Migraine From Tension-Type Headache

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