Distinct Proteomic, Transcriptomic, and Epigenetic Stress Responses in Dorsal and Ventral Hippocampus

Floriou-Servou, Amalia; Ziegler, Lukas von; Stalder, Luzia; Sturman, Oliver; Privitera, Mattia; Rassi, Anahita; Cremonesi, Alessio; Thöny, Beat; Bohacek, Johannes

doi:10.1016/j.biopsych.2018.02.003

Cited by 125 publications

(137 citation statements)

References 79 publications

(100 reference statements)

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“…Several studies have previously reported regional and temporally selective IEG activation patterns (Kubik et al 2007). Recently aggregated evidence has made it clear that there is a marked differentiation in both constitutive and behavior-induced transcriptional and translational activity along the axis (Sotiriou et al 2005;Pandis et al 2006;Gusev et al 2005;Leonardo et al 2006;Thompson et al 2008;Dong et al 2009;Snyder et al 2011;Cembrowski et al 2016;Lee et al 2017;Chawla et al 2018;Floriou-Servou et al 2018). The present results extend this evidence indicating that physiological activity patterns can significantly shape transcriptional heterogeneity, which therefore may further support functional heterogeneity along the hippocampus long axis.…”

Section: Implications Of Iegs Expression For Spws Functionsupporting

confidence: 84%

“…These, represent endogenous mechanistic aspects of the more general concept of functional segregation along the dorsoventral axis of hippocampus postulating that specific behavioral functions can be ascribed to distinct segments along the hippocampal formation, usually and shortly expressed by a dichotomy between cognition and emotionality related processes undertaken by the dorsal (DH) and the ventral hippocampus (VH) respectively (Bannerman et al 2014;Strange et al 2014;Gulyaeva 2018). The recently revealed striking diversification in patterns of gene expression along the hippocampus (Sotiriou et al 2005;Pandis et al 2006;Gusev et al 2005;Leonardo et al 2006; Thompson et al 2008;Dong et al 2009;Snyder et al 2011;Cembrowski et al 2016;Lee et al 2017;Chawla et al 2018;Floriou-Servou et al 2018), may have profound functional implications for the hippocampal circuitry and the higher-level functional diversification along hippocampus. However, though some dorsal-ventral differences, for instance in synaptic and cell level have been successfully linked to molecular diversity along the hippocampus (Pandis et al 2006;Dubovyk and Manahan-Vaughan 2018a;Snyder et al 2011;Zhu et al 2018;Floriou-Servou et al 2018;Dubovyk and Manahan-Vaughan 2018b), the functional implications of diversified patterns of gene expression are largely unknown (Tushev and Schuman 2016).…”

Section: Introductionmentioning

confidence: 99%

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Increased molecular plasticity along the septotemporal axis of the hippocampus is associated with network functioning

Sotiriou

Angelatou

Papatheodoropoulos

2019

Preprint

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Molecular plasticity crucially supports adaptive cellular and network functioning in the brain. Variations in molecular plasticity may yield important differences in neuronal network dynamics between discrete brain subregions. In the present study we show that the gradual development of sharp waves (SPWs), a spontaneous network activity that is organized under normal in vitro conditions in the CA1 field of ventral but not dorsal hippocampal slices, is associated with region selective molecular reorganization. In particular, increased levels of mRNAs for specific GABA A receptor subunits (α1, β2, γ2) occurred in ventral hippocampal CA1 field during the development of SPWs. These mRNA changes were followed by a clear increase in GABA A receptor number in ventral hippocampus, as shown by [ 3 H]muscimol binding. An increase in mRNAs was also observed in dorsal slices for α2 and α5 subunits, not followed by quantitative GABA A receptor changes. Furthermore, full development of SPWs in the CA1 field (at 3 hours of slice maintenance in vitro) was followed by increased expression of immediate early genes c-fos and zif-268 in ventral hippocampal slices (measured at 5 hours in vitro). No change in c-fos and zif-268 levels is observed in the CA1 field of dorsal slices, which do not develop spontaneous activity. These results suggest that generation of SPWs could trigger specific molecular reorganization in the VH that may be related to the functional roles of SPWs. Correspondingly, the revealed increased potentiality of the ventral hippocampus for molecular reorganization may provide a clue to mechanisms that underlie the regulated emergence of SPWs along the longitudinal axis of the hippocampus. Furthermore, the present evidence suggests that dynamic tuning between spontaneous neuronal activity and molecular organization may importantly contribute to the functional segregation/heterogeneity seen along the hippocampus.

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Section: Implications Of Iegs Expression For Spws Functionsupporting

confidence: 84%

Section: Introductionmentioning

confidence: 99%

Increased molecular plasticity along the septotemporal axis of the hippocampus is associated with network functioning

Sotiriou

Angelatou

Papatheodoropoulos

2019

Preprint

View full text Add to dashboard Cite

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“…DREADDs viral expression (for both wt-hM3Dq and PVCre-hM4Di) was confirmed by m-Cherry staining using standard immunohistochemistry protocols (Notter et al, 2014, Floriou-Servou et al, 2018. Briefly, after the last MRI session mice were deeply anesthetized using a mixture of Ketamine (100mg/kg; Graeub, Switzerland), Xylazine (10mg/kg; Rompun, Bayer) and Acepromazine (2mg/kg; Fatro S.p.A, Italy) and transcardially perfused with 4% Paraformaldehyde (PFA, pH=7.4).…”

Section: Histological Evaluation Of Transfectionmentioning

confidence: 99%

Cortical excitation:inhibition imbalance causes abnormal brain network dynamics as observed in neurodevelopmental disorders

Markicevic

Fulcher

Lewis

et al. 2018

Preprint

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AbstractAbnormal brain development manifests itself at different spatial scales. However, whether abnormalities at the cellular level can be diagnosed from network activity measured withfunctional magnetic resonance imaging (fMRI) is largely unknown, yet of high clinical relevance. Here we applied fMRI while using chemogenetics to increase the excitation-to-inhibition ratio (E:I) within cortical microcircuits of the mouse brain, thereby mimicking a putative mechanism of neurodevelopmental disorders including autism. Increased E:I caused a significant reduction of long-range connectivity, irrespective of whether excitatory neurons were facilitated or inhibitory Parvalbumin interneurons were suppressed. Training a classifier on fMRI signals, we were able to accurately classify cortical areas exhibiting increased E:I. This classifier was validated in an independent cohort of Fmr1y/- knock-out mice, a model for autism with well-documented loss of Parvalbumin neurons and chronic alterations of E:I. Our findings demonstrate a promising novel approach towards inferring microcircuit abnormalities from macroscopic fMRI measurements.

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“…Novelty induces psychological stress and arousal (Feenstra et al, 1995), which often results in efficient memory formation in the daily life (Fenker et al, 2008). Such emotional signaling involves the hippocampus (Kaplan et al, 2014;Knight, 1996) and especially its ventral moiety (Floriou-Servou et al, 2018), whereas encoding of spatial memory has been extensively studied in the dorsal hippocampus (Buzsáki and Moser, 2013). However, functional distinction and interaction between the dorsal and ventral hippocampus largely remain elusive.…”

Section: Introductionmentioning

confidence: 99%

“…MCs in the ventral hippocampus have extensive bilateral projections to the dorsal DG (Blasco-Ibáñez and Freund, 1997;Fujise et al, 1997) (Figure 1A). Based on this anatomical finding and the preferential signaling of novelty in the ventral hippocampus (Floriou-Servou et al, 2018), we hypothesized that this long range excitatory pathway could convey novelty signals providing a critical excitatory input to dorsal GCs (Scharfman, 2016), facilitating contextual memory formation.…”

Section: Introductionmentioning

confidence: 99%

Novelty gates memory formation through ventro-dorsal hippocampal interaction

Fredes

Silva

Kobayashi

et al. 2019

Preprint

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Novelty facilitates formation of memories. The detection of novelty and storage of contextual memories are both mediated by the hippocampus, yet the mechanisms that link these two functions remain to be defined. Dentate granule cells (GCs) of the dorsal hippocampus fire upon novelty exposure forming engrams of contextual memory. However, their key excitatory inputs from the entorhinal cortex are not responsive to novelty and are insufficient to make dorsal GCs fire reliably. Here we uncover a powerful glutamatergic pathway to dorsal GCs from ventral hippocampal mossy cells (MCs) that relays novelty, and is necessary and sufficient for driving dorsal GCs activation. Furthermore, manipulation of ventral MCs activity bidirectionally regulates novelty-induced contextual memory acquisition. Our results show that ventral MCs activity controls memory formation through an intra-hippocampal interaction mechanism gated by novelty.

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Distinct Proteomic, Transcriptomic, and Epigenetic Stress Responses in Dorsal and Ventral Hippocampus

Abstract: These findings underscore the importance of considering dorsal and ventral hippocampus separately when conducting high-throughput molecular analyses, which has important implications for fundamental research as well as clinical studies.

Cited by 125 publications

References 79 publications

Increased molecular plasticity along the septotemporal axis of the hippocampus is associated with network functioning

Increased molecular plasticity along the septotemporal axis of the hippocampus is associated with network functioning

Cortical excitation:inhibition imbalance causes abnormal brain network dynamics as observed in neurodevelopmental disorders

Novelty gates memory formation through ventro-dorsal hippocampal interaction

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