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Environmental enrichment and social isolation modulate inhibitory transmission and plasticity in hippocampal area CA2

Environmental enrichment and social isolation modulate inhibitory transmission and plasticity in... Environmental factors are well‐accepted to play a complex and interdependent role with genetic factors in learning and memory. The goal of this study was to examine how environmental conditions altered synaptic plasticity in hippocampal area CA2. To do this, we housed adult mice for 3 weeks in an enriched environment (EE) consisting of a larger cage with running wheel, and regularly changed toys, tunnels and treats. We then performed whole‐cell or extracellular field recordings in hippocampal area CA2 and compared the synaptic plasticity from EE‐housed mice with slices from littermate controls housed in standard environment (SE). We found that the inhibitory transmission recruited by CA3 input stimulation in CA2 was significantly less plastic in EE conditions as compared to SE following an electrical tetanus. We demonstrate that delta‐opioid receptor (DOR) mediated plasticity is reduced in EE conditions by direct application of DOR agonist. We show that in EE conditions the overall levels of GABA transmission is reduced in CA2 cells by analyzing inhibition of ErbB4 receptor, spontaneous inhibitory currents and paired‐pulse ratio. Furthermore, we report that the effect of EE of synaptic plasticity can be rapidly reversed by social isolation. These results demonstrate how the neurons in hippocampal area CA2 are sensitive to environment and may lead to promising therapeutic targets. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Hippocampus Wiley

Environmental enrichment and social isolation modulate inhibitory transmission and plasticity in hippocampal area CA2

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Publisher
Wiley
Copyright
© 2022 Wiley Periodicals LLC.
ISSN
1050-9631
eISSN
1098-1063
DOI
10.1002/hipo.23478
Publisher site
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Abstract

Environmental factors are well‐accepted to play a complex and interdependent role with genetic factors in learning and memory. The goal of this study was to examine how environmental conditions altered synaptic plasticity in hippocampal area CA2. To do this, we housed adult mice for 3 weeks in an enriched environment (EE) consisting of a larger cage with running wheel, and regularly changed toys, tunnels and treats. We then performed whole‐cell or extracellular field recordings in hippocampal area CA2 and compared the synaptic plasticity from EE‐housed mice with slices from littermate controls housed in standard environment (SE). We found that the inhibitory transmission recruited by CA3 input stimulation in CA2 was significantly less plastic in EE conditions as compared to SE following an electrical tetanus. We demonstrate that delta‐opioid receptor (DOR) mediated plasticity is reduced in EE conditions by direct application of DOR agonist. We show that in EE conditions the overall levels of GABA transmission is reduced in CA2 cells by analyzing inhibition of ErbB4 receptor, spontaneous inhibitory currents and paired‐pulse ratio. Furthermore, we report that the effect of EE of synaptic plasticity can be rapidly reversed by social isolation. These results demonstrate how the neurons in hippocampal area CA2 are sensitive to environment and may lead to promising therapeutic targets.

Journal

Hippocampus – Wiley

Published: Nov 14, 2022

Keywords: environmental enrichment; hippocampal area CA2; inhibitory transmission; social isolation; synaptic plasticity

References

  • A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives
    Benes, F. M.; Kwok, E. W.; Vincent, S. L.; Todtenkopf, M. S.
  • Perineuronal nets suppress plasticity of excitatory synapses on CA2 pyramidal neurons
    Carstens, K. E.; Phillips, M. L.; Pozzo‐Miller, L.; Weinberg, R. J.; Dudek, S. M.
  • ErbB4 in parvalbumin‐positive interneurons is critical for neuregulin 1 regulation of long‐term potentiation
    Chen, Y.‐J.; Zhang, M.; Yin, D.‐M.; Wen, L.; Ting, A.; Wang, P.; Lu, Y.‐S.; Zhu, X.‐H.; Li, S.‐J.; Wu, C.‐Y.; Wang, X.‐M.; Lai, C.; Xiong, W.‐C.; Mei, L.; Gao, T.‐M.
  • Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico‐hippocampal loop
    Chevaleyre, V.; Siegelbaum, S. A.
  • Effects of environment on morphology of rat cerebral cortex and hippocampus
    Diamond, M. C.; Ingham, C. A.; Johnson, R. E.; Bennett, E. L.; Rosenzweig, M. R.
  • Difference in occipital cortical synapses from environmentally enriched, impoverished, and standard colony rats
    Diamond, M. C.; Lindner, B.; Johnson, R.; Bennett, E. L.; Rosenzweig, M. R.
  • Effects of environmental enrichment and impoverishment on rat cerebral cortex
    Diamond, M. C.; Rosenzweig, M. R.; Bennett, E. L.; Lindner, B.; Lyon, L.
  • Maturation of PNN and ErbB4 signaling in area CA2 during adolescence underlies the emergence of PV interneuron plasticity and social memory
    Domínguez, S.; Rey, C. C.; Therreau, L.; Fanton, A.; Massotte, D.; Verret, L.; Piskorowski, R. A.; Chevaleyre, V.
  • Early‐ and late‐born parvalbumin basket cell subpopulations exhibiting distinct regulation and roles in learning
    Donato, F.; Chowdhury, A.; Lahr, M.; Caroni, P.
  • Parvalbumin‐expressing basket‐cell network plasticity induced by experience regulates adult learning
    Donato, F.; Rompani, S. B.; Caroni, P.
  • Distribution of delta opioid receptor‐expressing neurons in the mouse hippocampus
    Erbs, E.; Faget, L.; Scherrer, G.; Kessler, P.; Hentsch, D.; Vonesch, J.‐L.; Matifas, A.; Kieffer, B. L.; Massotte, D.
  • Activity‐dependent gating of parvalbumin interneuron function by the perineuronal net protein brevican
    Favuzzi, E.; Marques‐Smith, A.; Deogracias, R.; Winterflood, C. M.; Sanchez‐Aguilera, A.; Mantoan, L.; Maeso, P.; Fernandes, C.; Ewers, H.; Rico, B.
  • Environmental enrichment and brain repair: Harnessing the therapeutic effects of cognitive stimulation and physical activity to enhance experience‐dependent plasticity
    Hannan, A. J.
  • Transformation of cortical and hippocampal neural circuit by environmental enrichment
    Hirase, H.; Shinohara, Y.
  • Molecular abnormalities of the hippocampus in severe psychiatric illness: Postmortem findings from the Stanley Neuropathology Consortium
    Knable, M. B.; Barci, B. M.; Webster, M. J.; Meador‐Woodruff, J.; Torrey, E. F.; Consortium, S. N.
  • Long‐term memory underlying hippocampus‐dependent social recognition in mice
    Kogan, J. H.; Frankland, P. W.; Silva, A. J.
  • Newborn mice form lasting CA2‐dependent memories of their mothers
    Laham, B. J.; Diethorn, E. J.; Gould, E.
  • Input‐timing‐dependent plasticity in the hippocampal CA2 region and its potential role in social memory
    Leroy, F.; Brann, D. H.; Meira, T.; Siegelbaum, S. A.
  • Sequential inhibitory plasticities in hippocampal area CA2 and social memory formation
    Loisy, M.; Bouisset, G.; Lopez, S.; Muller, M.; Spitsyn, A.; Duval, J.; Piskorowski, R. A.; Verret, L.; Chevaleyre, V.
  • The relative benefits of environmental enrichment on learning and memory are greater when stressed: A meta‐analysis of interactions in rodents
    Macartney, E. L.; Lagisz, M.; Nakagawa, S.
  • Novel role for mineralocorticoid receptors in control of a neuronal phenotype
    McCann, K. E.; Lustberg, D. J.; Shaughnessy, E. K.; Carstens, K. E.; Farris, S.; Alexander, G. M.; Radzicki, D.; Zhao, M.; Dudek, S. M.
  • Environmental enrichment and the brain
    Mohammed, A. H.; Zhu, S. W.; Darmopil, S.; Hjerling‐Leffler, J.; Ernfors, P.; Winblad, B.; Diamond, M. C.; Eriksson, P. S.; Bogdanovic, N.
  • Oxytocin neurons mediate the effect of social isolation via the VTA circuits
    Musardo, S.; Contestabile, A.; Knoop, M.; Baud, O.; Bellone, C.
  • Inhibitory plasticity permits the recruitment of CA2 pyramidal neurons by CA3(1,2,3)
    Nasrallah, K.; Piskorowski, R. A.; Chevaleyre, V.
  • Routing hippocampal information flow through parvalbumin interneuron plasticity in area CA2
    Nasrallah, K.; Therreau, L.; Robert, V.; Huang, A. J. Y.; McHugh, T. J.; Piskorowski, R. A.; Chevaleyre, V.
  • Enriched environments, experience‐dependent plasticity and disorders of the nervous system
    Nithianantharajah, J.; Hannan, A. J.
  • Delta‐opioid receptors mediate unique plasticity onto parvalbumin‐expressing interneurons in area CA2 of the hippocampus
    Piskorowski, R. A.; Chevaleyre, V.
  • Age‐dependent specific changes in area CA2 of the hippocampus and social memory deficit in a mouse model of the 22q11.2 deletion syndrome
    Piskorowski, R. A.; Nasrallah, K.; Diamantopoulou, A.; Mukai, J.; Hassan, S. I.; Siegelbaum, S. A.; Gogos, J. A.; Chevaleyre, V.
  • Altered inhibitory function in hippocampal CA2 contributes in social memory deficits in Alzheimer's mouse model
    Rey, C. C.; Robert, V.; Bouisset, G.; Loisy, M.; Lopez, S.; Cattaud, V.; Lejards, C.; Piskorowski, R. A.; Rampon, C.; Chevaleyre, V.; Verret, L.
  • Experience enhances gamma oscillations and interhemispheric asymmetry in the hippocampus
    Shinohara, Y.; Hosoya, A.; Hirase, H.
  • Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model
    Verret, L.; Mann, E. O.; Hang, G. B.; Barth, A. M. I.; Cobos, I.; Ho, K.; Devidze, N.; Masliah, E.; Kreitzer, A. C.; Mody, I.; Mucke, L.; Palop, J. J.
  • Neuregulin‐1 enhances depolarization‐induced GABA release
    Woo, R.‐S.; Li, X.‐M.; Tao, Y.; Carpenter‐Hyland, E.; Huang, Y. Z.; Weber, J.; Neiswender, H.; Dong, X.‐P.; Wu, J.; Gassmann, M.; Lai, C.; Xiong, W.‐C.; Gao, T.‐M.; Mei, L.
  • Synaptic plasticity (and the lack thereof) in hippocampal CA2 neurons
    Zhao, M.; Choi, Y.‐S.; Obrietan, K.; Dudek, S. M.