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Differential impact of chronic stress along the hippocampal dorsal–ventral axis

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Abstract

Stress impacts differently in distinct brain regions. However, so far few studies have focused on the differential responses triggered by stressful stimuli on the intrinsic functional heterogeneity of the hippocampal axis. In this study, we assessed the functional and structural alterations caused by exposure to a chronic unpredictable stress (CUS) paradigm on the dorsal–ventral axis of the hippocampus. The morphological analysis demonstrated that CUS had opposite outcomes in the structure of the dorsal (DH) and ventral hippocampus (VH): whereas in the DH, stress triggered a volumetric reduction as a result of atrophy of CA3 and CA1 apical dendrites, in the VH there was an increase in hippocampal volume concurrent with the increase of CA3 apical dendrites. In parallel, electrophysiological data revealed that stress led to a decrease in VH LTD. In summary, the present work showed that stress impacts differently on the structure and function of the DH and VH which contributes to better understand the overall spectrum of the central effects of stress.

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References

  • Ambrogi Lorenzini C, Bucherelli C, Giachetti A, Tassoni G (1987) Spontaneous and conditioned behavior of Wistar and Long Evans rats. Arch Ital Biol 125:155–170

    CAS  PubMed  Google Scholar 

  • Anderson WW, Collingridge GL (2007) Capabilities of the WinLTP data acquisition program extending beyond basic LTP experimental functions. J Neurosci Methods 162:346–356

    Article  PubMed  Google Scholar 

  • Bastrikova N, Gardner GA, Reece JM, Jeromin A, Dudek SM (2008) Synapse elimination accompanies functional plasticity in hippocampal neurons. Proc Natl Acad Sci USA 105:3123–3127

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bear MF, Abraham WC (1996) Long-term depression in hippocampus. Annu Rev Neurosci 19:437–462

    Article  CAS  PubMed  Google Scholar 

  • Bear MF, Cooper LN, Ebner FF (1987) A physiological basis for a theory of synapse modification. Science 237:42–48

    Article  CAS  PubMed  Google Scholar 

  • Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39

    Article  CAS  PubMed  Google Scholar 

  • Cerqueira JJ, Mailliet F, Almeida OF, Jay TM, Sousa N (2007) The prefrontal cortex as a key target of the maladaptive response to stress. J Neurosci 27:2781–2787

    Article  CAS  PubMed  Google Scholar 

  • Citri A, Malenka RC (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33:18–41

    Article  PubMed  Google Scholar 

  • Colgin LL, Kubota D, Jia Y, Rex CS, Lynch G (2004) Long-term potentiation is impaired in rat hippocampal slices that produce spontaneous sharp waves. J Physiol 558:953–961

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dias-Ferreira E, Sousa JC, Melo I, Morgado P, Mesquita AR, Cerqueira JJ, Costa RM, Sousa N (2009) Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325:621–625

    Article  CAS  PubMed  Google Scholar 

  • Dorey R, Piérard C, Chauveau F, David V, Béracochéa D (2012) Stress-induced memory retrieval impairments: different time-course involvement of corticosterone and glucocorticoid receptors in dorsal and ventral hippocampus. Neuropsychopharmacology 37:2870–2880

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7–19

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Godsil BP, Kiss JP, Spedding M, Jay TM (2013) The hippocampal–prefrontal pathway: the weak link in psychiatric disorders? Eur Neuropsychopharmacol 23:1165–1181

    Article  CAS  PubMed  Google Scholar 

  • Hawley DF, Leasure JL (2012) Region-specific response of the hippocampus to chronic unpredictable stress. Hippocampus 22:1338–1349

    Article  PubMed  Google Scholar 

  • Hawley DF, Morch K, Christie BR, Leasure JL (2012) Differential response of hippocampal subregions to stress and learning. PLoS ONE 7:e53126

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hessler NA, Shirke AM, Malinow R (1993) The probability of transmitter release at a mammalian central synapse. Nature 366:569–572

    Article  CAS  PubMed  Google Scholar 

  • Krugers HJ, Alfarez DN, Karst H, Parashkouhi K, van Gemert N, Joëls M (2005) Corticosterone shifts different forms of synaptic potentiation in opposite directions. Hippocampus 15:697–703

    Article  CAS  PubMed  Google Scholar 

  • Luine V, Villegas M, Martinez C, McEwen BS (1994) Repeated stress causes reversible impairments of spatial memory performance. Brain Res 639:167–170

    Article  CAS  PubMed  Google Scholar 

  • Luine V, Martinez C, Villegas M, Magariños AM, McEwen BS (1996) Restraint stress reversibly enhances spatial memory performance. Physiol Behav 59:27–32

    Article  CAS  PubMed  Google Scholar 

  • Maggio N, Segal M (2007) Striking variations in corticosteroid modulation of long-term potentiation along the septotemporal axis of the hippocampus. J Neurosci 27:5757–5765

    Article  CAS  PubMed  Google Scholar 

  • Maruki K, Izaki Y, Nomura M, Yamauchi T (2001) Differences in paired-pulse facilitation and long-term potentiation between dorsal and ventral CA1 regions in anesthetized rats. Hippocampus 11:655–661

    Article  CAS  PubMed  Google Scholar 

  • McEwen BS (2012) The ever-changing brain: cellular and molecular mechanisms for the effects of stressful experiences. Dev Neurobiol 72:878–890

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McHugh SB, Fillenz M, Lowry JP, Rawlins JN, Bannerman DM (2011) Brain tissue oxygen amperometry in behaving rats demonstrates functional dissociation of dorsal and ventral hippocampus during spatial processing and anxiety. Eur J Neurosci 33:322–337

    Article  PubMed Central  PubMed  Google Scholar 

  • Moser MB, Moser EI (1998) Functional differentiation in the hippocampus. Hippocampus 8:608–619

    Article  CAS  PubMed  Google Scholar 

  • Naber PA, Witter MP (1998) Subicular efferents are organized mostly as parallel projections: a double-labeling, retrograde-tracing study in the rat. J Comp Neurol 393:284–297

    Article  CAS  PubMed  Google Scholar 

  • Oliveira JF, Dias NS, Correia M, Gama-Pereira F, Sardinha VM, Lima A, Oliveira AF, Jacinto LR, Ferreira DS, Silva AM, Reis JS, Cerqueira JJ, Sousa N (2013) Chronic stress disrupts neural coherence between cortico-limbic structures. Front Neural Circuits 7:1–10

    Google Scholar 

  • Papatheodoropoulos C, Kostopoulos G (2000a) Decreased ability of rat temporal hippocampal CA1 region to produce long-term potentiation. Neurosci Lett 279:177–180

    Article  CAS  PubMed  Google Scholar 

  • Papatheodoropoulos C, Kostopoulos G (2000b) Dorsal–ventral differentiation of short-term synaptic plasticity in rat CA1 hippocampal region. Neurosci Lett 286:57–60

    Article  CAS  PubMed  Google Scholar 

  • Pavlides C, McEwen BS (1999) Effects of mineralocorticoid and glucocorticoid receptors on long-term potentiation in the CA3 hippocampal field. Brain Res 851:204–214

    Article  CAS  PubMed  Google Scholar 

  • Pêgo JM, Morgado P, Pinto LG, Cerqueira JJ, Almeida OF, Sousa N (2008) Dissociation of the morphological correlates of stress-induced anxiety and fear. Eur J Neurosci 27:1503–1516

    Article  PubMed  Google Scholar 

  • Rajah MN, Kromas M, Han JE, Pruessner JC (2010) Group differences in anterior hippocampal volume and in the retrieval of spatial and temporal context memory in healthy young versus older adults. Neuropsychologia 48:4020–4030

    Article  PubMed  Google Scholar 

  • Sapolsky RM, Krey LC, McEwen BS (1985) Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J Neurosci 5:1222–1227

    CAS  PubMed  Google Scholar 

  • Segal M, Richter-Levin G, Maggio N (2010) Stress-induced dynamic routing of hippocampal connectivity: a hypothesis. Hippocampus 20:1332–1338

    Article  PubMed  Google Scholar 

  • Sotiropoulos I, Cerqueira JJ, Catania C, Takashima A, Sousa N, Almeida OF (2008) Stress and glucocorticoid footprints in the brain-the path from depression to Alzheimer’s disease. Neurosci Biobehav Rev 32:1161–1173

    Article  CAS  PubMed  Google Scholar 

  • Sousa N, Almeida OF (2012) Disconnection and reconnection: the morphological basis of (mal)adaptation to stress. Trends Neurosci 35:742–751

    Article  CAS  PubMed  Google Scholar 

  • Sousa N, Cerqueira JJ, Almeida OF (2008) Corticosteroid receptors and neuroplasticity. Brain Res Rev 57:561–570

    Article  CAS  PubMed  Google Scholar 

  • Swanson LW, Wyss JM, Cowan WM (1978) An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181:681–715

    Article  CAS  PubMed  Google Scholar 

  • Wang XB, Yang Y, Zhou Q (2007) Independent expression of synaptic and morphological plasticity associated with long-term depression. J Neurosci 27:12419–12429

    Article  CAS  PubMed  Google Scholar 

  • Witter MP, Amaral DG (2004) The hippocampal formation. In: Paxinos G (ed) The rat nervous system. Academic Press, San Diego, pp 635–704

    Google Scholar 

  • Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355–405

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Pinto V and Mota C were supported by Fundação para a Ciência e Tecnologia (FCT) grants (SFRH/BPD/69132/2010; SFRH/BD/81881/2011, respectively). This work was supported by an FCT grant (PTDC/SAU-NSC/120590/2010). The authors declare no competing financial interests.

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Authors and Affiliations

  1. Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, Braga, Portugal

    V. Pinto, J. C. Costa, P. Morgado, C. Mota, A. Miranda, F. V. Bravo, T. G. Oliveira, J. J. Cerqueira & N. Sousa

  2. ICVS/3B’s-PT Government Associate Laboratory, Braga/Guimarães, Portugal

    V. Pinto, J. C. Costa, P. Morgado, C. Mota, A. Miranda, F. V. Bravo, T. G. Oliveira, J. J. Cerqueira & N. Sousa

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  1. V. Pinto
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  2. J. C. Costa
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  3. P. Morgado
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  4. C. Mota
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  5. A. Miranda
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  7. T. G. Oliveira
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  8. J. J. Cerqueira
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  9. N. Sousa
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Correspondence to N. Sousa.

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Pinto, V., Costa, J.C., Morgado, P. et al. Differential impact of chronic stress along the hippocampal dorsal–ventral axis. Brain Struct Funct 220, 1205–1212 (2015). https://doi.org/10.1007/s00429-014-0713-0

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  • DOI: https://doi.org/10.1007/s00429-014-0713-0

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