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The effect of a caudal hippocampus lesion on learning in a Morris water maze in Bank Voles (Clethrionomys glareolus)

  • Animal and Human Physiology
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Abstract

The involvement of the caudal hippocampus in spatial learning is presently uncertain, compared to the well established role of the dorsal region. Therefore voles (Clethrionomys glareolus) with large (about 1/3 of the whole hippocampus) caudal cytotoxic lesions were tested in the Morris water maze. A version of the test intended to measure long term spatial memory was used. The lesion inhibited the learning process, as well as reducing the accuracy of platform location memory at early stages of training. The data obtained indicate the involvement of this area in control of spatial learning in rodents.

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References

  • Amaral, D.G. and Witter, M.P., The Three-Dimensional Organization of the Hippocampal Formation: A Review of Anatomical Data, Neuroscience, 1989, vol. 31, pp. 571–591.

    Article  PubMed  CAS  Google Scholar 

  • Bannerman, D.M., Yee, B.K., Good, M.A., et al., Double Dissociation of Function within the Hippocampus: A Comparison of Dorsal, Ventral, and Complete Hippocampal Cytotoxic Lesions, Behav. Neurosci., 1999, vol. 113, no. 6, pp. 1170–1188.

    Article  PubMed  CAS  Google Scholar 

  • Bannerman, D.M., Rawlins, J.N., McHugh, S.B., et al., Regional Dissociations within the Hippocampus-Memory and Anxiety, Neurosci. Biobehav. Rev., 2004, vol. 28, no. 3, pp. 273–283.

    Article  PubMed  CAS  Google Scholar 

  • Bast, T., Toward an Integrative Perspective on Hippocampal Function: From the Rapid Encoding of Experience to Adaptive Behavior, Rev. Neurosci., 2007, vol. 18, nos. 3–4, pp. 253–281.

    PubMed  Google Scholar 

  • Bast, T., Wilson, I.A., Witter, M.P., and Morris, R.G., From Rapid Place Learning to Behavioral Performance: A Key Role for the Intermediate Hippocampus, PLoS Biol., 2009, vol. 7, no. 4, p. e1000089.

    Article  PubMed  Google Scholar 

  • Czerniawski, J., Yoon, T., and Otto, T., Dissociating Space and Trace in Dorsal and Ventral Hippocampus, Hippocampus, 2009, vol. 19, no. 1, pp. 20–32.

    Article  PubMed  Google Scholar 

  • Deacon, R.M., Croucher, A., and Rawlins, J.N., Hippocampal Cytotoxic Lesion Effects on Species-Typical Behaviours in Mice, Behav. Brain Res., 2002, vol. 132, no. 2, pp. 203–213.

    Article  PubMed  Google Scholar 

  • Fanselow, M.S. and Dong, H.W., Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures?, Neuron, 2010, vol. 65, no. 1, pp. 7–19.

    Article  PubMed  CAS  Google Scholar 

  • Ferbinteanu, J., Ray, C., and McDonald, R.J., Both Dorsal and Ventral Hippocampus Contribute to Spatial Learning in Long-Evans Rats, Neurosci. Lett., 2003, vol. 345, no. 2, pp. 131–135.

    Article  PubMed  CAS  Google Scholar 

  • Ferino, F., Thierry, A.M., and Glowinski, J., Anatomical and Electrophysiological Evidence for a Direct Projection from Ammon’s Horn to the Medial Prefrontal Cortex in the Rat, Exp. Brain Res., 1987, vol. 65, no. 2, pp. 421–426.

    Article  PubMed  CAS  Google Scholar 

  • Hok, V., Lenck-Santini, P.P., Save, E., et al., A Test of the Time Estimation Hypothesis of Place Cell Goal-Related Activity, J. Integr. Neurosci., 2007, vol. 6, no. 3, pp. 367–378.

    Article  PubMed  Google Scholar 

  • de Hoz, L., Knox, J., and Morris, R.G., Longitudinal Axis of the Hippocampus: Both Septal and Temporal Poles of the Hippocampus Support Water Maze Spatial Learning Depending on the Training Protocol, Hippocampus, 2003, vol. 13, no. 5, pp. 587–603.

    Article  PubMed  Google Scholar 

  • Jung, M.W., Wiener, S.I., and McNaughton, B.L., Comparison of Spatial Firing Characteristics of Units in Dorsal and Ventral Hippocampus of the Rat, J. Neurosci., 1994, vol. 14, no. 12, pp. 7347–7356.

    PubMed  CAS  Google Scholar 

  • Kerr, K.M., Agster, K.L., Furtak, S.C., and Burwell, R.D., Functional Neuroanatomy of the Parahippocampal Region: The Lateral and Medial Entorhinal Areas, Hippocampus, 2007, vol. 17, no. 9, pp. 697–708.

    Article  PubMed  Google Scholar 

  • Kjelstrup, K.G., Tuvnes, F.A., Steffenach, H.A., et al., Reduced Fear Expression after Lesions of the Ventral Hippocampus, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, no. 16, pp. 10825–10830.

    Article  PubMed  CAS  Google Scholar 

  • Kjelstrup, K.B., Solstad, T., Brun, V.H., et al., Finite Scale of Spatial Representation in the Hippocampus, Science, 2008, vol. 321, no. 5885, pp. 140–143.

    Article  PubMed  CAS  Google Scholar 

  • Kuptsov, P.A., Pleskacheva, M.G., Voronkov, D.N., et al., Features of the c-Fos Gene Expression along the Hippocampal Rostro-Caudal Axis in Common Voles after Rapid Spatial Learning, Zh. Vyssh. Nervn. Deyat., 2005, vol. 55, no. 2, pp. 231–240.

    CAS  Google Scholar 

  • Kuptsov, P.A., Pleskacheva, M.G., and Anokhin, K.V., Inhomogeneous Hippocampal Activation along the Rostrocaudal Axis in Mice after Exploration of Novel Environment, Zh. Vyssh. Nervn. Deyat., 2012, vol. 62, no. 1, pp. 43–55.

    CAS  Google Scholar 

  • Loureiro, M., Lecourtier, L., Engeln, M., et al., The Ventral Hippocampus Is Necessary for Expressing a Spatial Memory, Brain Struct. Funct., 2012, vol. 217, no. 1, pp. 93–106.

    Article  PubMed  Google Scholar 

  • McHugh, S.B., Fillenz, M., Lowry, J.P., et al., Brain Tissue Oxygen Amperometry in Behaving Rats Demonstrates Functional Dissociation of Dorsal and Ventral Hippocampus during Spatial Processing and Anxiety, Eur. J. Neurosci., 2011, vol. 33, no. 2, pp. 322–337.

    Article  PubMed  Google Scholar 

  • Morris, R.G., Garrud, P., Rawlins, J.N., and O’Keefe, J., Place Navigation Impaired in Rats with Hippocampal Lesions, Nature, 1982, vol. 297, pp. 681–683.

    Article  PubMed  CAS  Google Scholar 

  • Morris, R., Developments of a Water-Maze Procedure for Studying Spatial Learning in the Rat, J. Neurosci. Methods, 1984, vol. 11, no. 1, pp. 47–60.

    Article  PubMed  CAS  Google Scholar 

  • Moser, E.I., Moser, M.B., and Andersen, P., Spatial Learning Impairment Parallels the Magnitude of Dorsal Hippocampal Lesions, but Is Hardly Present Following Ventral Lesions, J. Neurosci., 1993, vol. 13, no. 9, pp. 3916–3925.

    PubMed  CAS  Google Scholar 

  • Moser, M.B., Moser, E.I., Forrest, E., et al., Spatial Learning with a Minislab in the Dorsal Hippocampus, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, no. 21, pp. 9697–9701.

    Article  PubMed  CAS  Google Scholar 

  • Moser, M.B. and Moser, E.I., Functional Differentiation in the Hippocampus, Hippocampus, 1998, vol. 8, no. 6, pp. 608–619.

    Article  PubMed  CAS  Google Scholar 

  • Moser, E.I., Kropff, E., and Moser, M.B., Place Cells, Grid Cells, and the Brain’s Spatial Representation System, Annu. Rev. Neurosci., 2008, vol. 31, pp. 69–89.

    Article  PubMed  CAS  Google Scholar 

  • O’Keefe, J. and Nadel, L., The Hippocampus as a Cognitive Map, Oxford: Oxford Univ. Press, 1978.

    Google Scholar 

  • Pleskacheva, M.G., Wolfer, D.P., Kupriyanova, I.F., et al., Hippocampal Mossy Fibers and Swimming Navigation Learning in Two Vole Species Occupying Different Habitats, Hippocampus, 2000, vol. 10, no. 1, pp. 17–30.

    Article  PubMed  CAS  Google Scholar 

  • Poucet, B., Thinus-Blanc, C., and Muller, R.U., Place Cells in the Ventral Hippocampus of Rats, Neuroreport, 1994, vol. 5, no. 16, pp. 2045–2048.

    Article  PubMed  CAS  Google Scholar 

  • Richmond, M.A., Yee, B.K., Pouzet, B., et al., Dissociating Context and Space within the Hippocampus: Effects of Complete, Dorsal, and Ventral Excitotoxic Hippocampal Lesions on Conditioned Freezing and Spatial Learning, Behav. Neurosci., 1999, vol. 113, no. 6, pp. 1189–1203.

    Article  PubMed  CAS  Google Scholar 

  • Royer, S., Sirota, A., Patel, J., and Buzsaki, G., Distinct Representations and Theta Dynamics in Dorsal and Ventral Hippocampus, J. Neurosci., 2010, vol. 30, no. 5, pp. 1777–1787.

    Article  PubMed  CAS  Google Scholar 

  • Silachev, D.N., Shram, S.I., Shakova, F.M., et al., Formation of Spatial Memory in Rats with Ischemic Lesions to the Prefrontal Cortex; Effects of a Synthetic Analog of ACTH(4-7), Neurosci. Behav. Physiol., 2009, vol. 39, no. 8, pp. 749–756.

    Article  PubMed  CAS  Google Scholar 

  • Vandebroek, I., Bouche, K., D’Herde, K., et al., A Stereotaxic Atlas of the Forebrain of the Bank Vole (Clethrionomys glareolus), Brain Res. Bull., 1999, vol. 48, no. 6, pp. 555–567.

    Article  PubMed  CAS  Google Scholar 

  • Vann, S.D., Brown, M.W., Erichsen, J.T., and Aggleton, J.P., Fos Imaging Reveals Differential Patterns of Hippocampal and Parahippocampal Subfield Activation in Rats in Response to Different Spatial Memory Tests, J. Neurosci., 2000, vol. 20, no. 7, pp. 2711–2718.

    PubMed  CAS  Google Scholar 

  • Vinogadova, O.S., Gippokamp i pamyat’ (Hippocampus and Memory), Moscow: Nauka, 1975.

    Google Scholar 

  • Wolfer, D.P., Madani, R., Valenti, P., and Lipp, H.P., Extended Analysis of Path Data from Mutant Mice Using the Public Domain Software Wintrack, Physiol. Behav., 2001, vol. 73, no. 5, pp. 745–753.

    Article  PubMed  CAS  Google Scholar 

  • Yartsev, M.M., Distinct or Gradually Changing Spatial and Nonspatial Representations along the Dorsoventral Axis of the Hippocampus, J. Neurosci., 2010, vol. 30, no. 23, pp. 7758–7760.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to I. V. Lebedev.

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Original Russian Text © I.V. Lebedev, D.V. Bezryadnov, R.M.J. Deacon, P.A. Kuptsov, V.M. Malygin, M.G. Pleskacheva, 2013, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2013, No. 2, pp. 197–205.

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Lebedev, I.V., Bezryadnov, D.V., Deacon, R.M.J. et al. The effect of a caudal hippocampus lesion on learning in a Morris water maze in Bank Voles (Clethrionomys glareolus). Biol Bull Russ Acad Sci 40, 179–186 (2013). https://doi.org/10.1134/S1062359013020088

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  • DOI: https://doi.org/10.1134/S1062359013020088

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