Skip to main content
SpringerLink
Log in

The hippocampal to prefrontal cortex circuit in mice: a promising electrophysiological signature in models for psychiatric disorders

  • Short Communication
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Interaction between the hippocampus and the medial prefrontal cortex (mPFC) has been identified as a key target in several neuropsychiatric disorders. However, the hippocampus–mPFC (H-PFC) pathway has not been outlined in mice, which are increasingly the leading choice for new animal models for neurological disorders. Our results, establish the existence of a topographical, monosynaptic pathway originating exclusively from the ventral CA1 and subiculum to the mPFC. Functional connectivity of the H-PFC pathway, examined in vivo through field potential recordings in the prelimbic mPFC after high-frequency stimulation of the hippocampal outflow, demonstrates an induction of a significant long lasting long-term potentiation, which is stable for at least one hour and strongly impaired by exposure to acute stress. Given that stress exposure is known to have serious detrimental effects on prefrontal cortical functioning and is considered a major risk factor for several neuropsychiatric disorders, the present study provides a crucial animal model of neural interaction and response to environmental stress which could lend itself to the study of disruption of brain circuits and test for potential drug candidates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

References

  • Barker GR, Warburton EC (2011) Evaluating the neural basis of temporal order memory for visual stimuli in the rat. Eur J Neurosci 33(4):705–716. doi:10.1111/j.1460-9568.2010.07555.x

    Article  CAS  PubMed  Google Scholar 

  • Benchenane K, Peyrache A, Khamassi M, Tierney PL, Gioanni Y, Battaglia FP, Wiener SI (2010) Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 66(6):921–936. doi:10.1016/j.neuron.2010.05.013

    Article  CAS  PubMed  Google Scholar 

  • Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31–39. doi:10.1038/361031a0

    Article  CAS  PubMed  Google Scholar 

  • Cenquizca LA, Swanson LW (2007) Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res Rev 56(1):1–26. doi:10.1016/j.brainresrev.2007.05.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Floresco SB, Seamans JK, Phillips AG (1997) Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J Neurosci 17(5):1880–1890

    CAS  PubMed  Google Scholar 

  • Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6(2):119–130

    Article  CAS  PubMed  Google Scholar 

  • Franklin KBJ, Paxinos G (2008) The mouse brain in stereotaxic coordinates. 3rd edn. Elsevier, San Diego

  • Garcia R, Musleh W, Tocco G, Thompson RF, Baudry M (1997) Time-dependent blockade of STP and LTP in hippocampal slices following acute stress in mice. Neurosci Lett 233(1):41–44 (pii: S0304-3940(97)00621-6)

    Article  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(10):1165–1181. doi:10.1016/j.euroneuro.2012.10.018

    Article  CAS  PubMed  Google Scholar 

  • Jay TM, Witter MP (1991) Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 313(4):574–586. doi:10.1002/cne.903130404

    Article  CAS  PubMed  Google Scholar 

  • Jay TM, Glowinski J, Thierry AM (1989) Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res 505(2):337–340 (pii: 0006-8993(89)91464-9)

    Article  CAS  PubMed  Google Scholar 

  • Jay TM, Burette F, Laroche S (1996) Plasticity of the hippocampal-prefrontal cortex synapses. J Physiol Paris 90(5–6):361–366 (pii: S0928-4257(97)87920-X)

    Article  CAS  PubMed  Google Scholar 

  • Killcross S, Coutureau E (2003) Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13(4):400–408

    Article  PubMed  Google Scholar 

  • Laroche S, Jay TM, Thierry AM (1990) Long-term potentiation in the prefrontal cortex following stimulation of the hippocampal CA1/subicular region. Neurosci Lett 114(2):184–190 (pii: 0304-3940(90)90069-L)

    Article  CAS  PubMed  Google Scholar 

  • Li S, Fan YX, Wang W, Tang YY (2012) Effects of acute restraint stress on different components of memory as assessed by object-recognition and object-location tasks in mice. Behav Brain Res 227(1):199–207. doi:10.1016/j.bbr.2011.10.007

    Article  PubMed  Google Scholar 

  • McNamara RK, Namgung U, Routtenberg A (1996) Distinctions between hippocampus of mouse and rat: protein F1/GAP-43 gene expression, promoter activity, and spatial memory. Brain Res Mol Brain Res 40(2):177–187 (pii: 0169328X96000484)

    Article  CAS  PubMed  Google Scholar 

  • Murphy BL, Arnsten AF, Jentsch JD, Roth RH (1996) Dopamine and spatial working memory in rats and monkeys: pharmacological reversal of stress-induced impairment. J Neurosci 16(23):7768–7775

    CAS  PubMed  Google Scholar 

  • O’Neill PK, Gordon JA, Sigurdsson T (2013) Theta oscillations in the medial prefrontal cortex are modulated by spatial working memory and synchronize with the hippocampus through its ventral subregion. J Neurosci 33(35):14211–14224. doi:10.1523/JNEUROSCI.2378-13.2013

    Article  PubMed  PubMed Central  Google Scholar 

  • Rocher C, Spedding M, Munoz C, Jay TM (2004) Acute stress-induced changes in hippocampal/prefrontal circuits in rats: effects of antidepressants. Cereb Cortex 14(2):224–229

    Article  PubMed  Google Scholar 

  • Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36(2):529–538. doi:10.1038/npp.2010.184

    Article  PubMed  PubMed Central  Google Scholar 

  • Swanson LW (1981) A direct projection from Ammon’s horn to prefrontal cortex in the rat. Brain Res 217(1):150–154 (pii: 0006-8993(81)90192-X)

    Article  CAS  PubMed  Google Scholar 

  • Van De Werd HJ, Rajkowska G, Evers P, Uylings HB (2010) Cytoarchitectonic and chemoarchitectonic characterization of the prefrontal cortical areas in the mouse. Brain Struct Funct 214(4):339–353. doi:10.1007/s00429-010-0247-z

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The research leading to these results were performed in conjunction with the European Community’s Seventh framework program (FP7/2007-2013) for the Innovative Medicine Initiative under Grant Agreement No. 115008.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Compliance with ethical standard

All applicable institutional guidelines conforming to animal experimentation were followed during this study. All experiments were ethically reviewed and carried out in accordance with French (Decree No. 87/848) and European (86/609/EEC) legislation regarding use and care of laboratory animals. The protocols have been approved by the Comité d’Éthique en Expérimentation Animale No. 34, Ministère de l’Enseignement Supérieur et de la Recherche, under protocol ID 00713.03.

Author information

Authors and Affiliations

  1. Physiopathogie des Maladies Psychiatriques, INSERM UMR_S 894, Centre de Psychiatrie et Neurosciences, 2ter rue d’Alesia, 75014, Paris, France

    Anushree Tripathi & Therese M. Jay

  2. Université Paris Descartes, Sorbonne Paris Cité, Paris, France

    Anushree Tripathi & Therese M. Jay

  3. Institut de Recherches Servier, Croissy, France

    Esther Schenker & Michael Spedding

Authors
  1. Anushree Tripathi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Esther Schenker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Spedding
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Therese M. Jay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Therese M. Jay.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tripathi, A., Schenker, E., Spedding, M. et al. The hippocampal to prefrontal cortex circuit in mice: a promising electrophysiological signature in models for psychiatric disorders. Brain Struct Funct 221, 2385–2391 (2016). https://doi.org/10.1007/s00429-015-1023-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-015-1023-x

Keywords

Search

Navigation