Skip to main content
Log in

Exploratory and Locomotor Activity in Mice Following Selective Lesions of the Hippocampus: Effects of Lesion Site and Open Field Arena Size

  • Experimental Papers
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

The present study showed arena size-dependent effects on the impairment of locomotor activity and rearing after lesions of caudal hippocampus in C57BL/6 mice: intensive high-speed locomotion without intra- and intertrial habituation accompanied by a decreased number of rears and a reduced tortuosity of the route, suggesting significant impairments of exploratory behavior in an unfamiliar large environment. The lesions of the rostral hippocampus resulted in slight hyperactivity in the large arena without impairment of habituation or rearing. The caudal hippocampus is thus crucial for the environment-dependent modifications of exploratory behavior. Changes on exploratory behavior after its lesions are similar to ones following more extensive or complete lesions of the hippocampus.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

REFERENCES

  1. Bannerman DM, Rawlins JN, McHugh SB, et al. (2004) Regional dissociations within the hippocampus—memory and anxiety. Neurosci Biobehav Rev 28: 273–283. https://doi.org/10.1016/j.neubiorev.2004.03.004

  2. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65: 7–19. https://doi.org/10.1016/j.neuron.2009.11.031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Strange BA, Witter MP, Lein ES, Moser EI (2014) Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 15: 655–669. https://doi.org/10.1038/nrn3785

    Article  CAS  PubMed  Google Scholar 

  4. Harland B, Contreras M, Fellous J-M (2017) A role for the longitudinal axis of the hippocampus in multiscale representations of large and complex spatial environments and mnemonic hierarchies. In: Stuchlik A (Ed) The Hippocampus—Plasticity and Functions. pp. 67–104. https://doi.org/10.5772/intechopen.71165

    Chapter  Google Scholar 

  5. Dougherty KA (2020) Differential developmental refinement of the intrinsic electrophysiological properties of CA1 pyramidal neurons from the rat dorsal and ventral hippocampus. Hippocampus 30: 233–249. https://doi.org/10.1002/hipo.23152

    Article  CAS  PubMed  Google Scholar 

  6. Lothmann K, Deitersen J, Zilles K, Amunts K, Herold C (2021) New boundaries and dissociation of the mouse hippocampus along the dorsal-ventral axis based on glutamatergic, GABAergic and catecholaminergic receptor densities. Hippocampus 31: 56–78. https://doi.org/10.1002/hipo.23262

    Article  CAS  PubMed  Google Scholar 

  7. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press.

    Google Scholar 

  8. Rawlins JN, Lyford GL, Seferiades A, Deacon RM, Cassaday HJ (1993) Critical determinants of nonspatial working memory deficits in rats with conventional lesions of the hippocampus or fornix. Behav Neurosci 107: 420–433.

    Article  CAS  PubMed  Google Scholar 

  9. Cassaday HJ, Rawlins JN (1995) Fornix-fimbria section and working memory deficits in rats: stimulus complexity and stimulus size. Behav Neurosci 109: 594–606.

    Article  CAS  PubMed  Google Scholar 

  10. Cassaday HJ, Rawlins JN (1997) The hippocampus, objects, and their contexts. Behav Neurosci 111: 1228–1244.

    Article  CAS  PubMed  Google Scholar 

  11. Bast T (2007) Toward an integrative perspective on hippocampal function: from the rapid encoding of experience to adaptive behavior. Rev Neurosci 18: 253–281.

    Article  PubMed  Google Scholar 

  12. Moser E, Moser MB, Andersen P (1993) Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J Neurosci 13: 3916–3925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Moser MB, Moser EI, Forrest E, Andersen P, Morris RG (1995) Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci USA 92: 9697–9701. https://doi.org/10.1073/pnas.92.21.9697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, Rawlins JN (1999) Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci 113: 1170–1188.

    Article  CAS  PubMed  Google Scholar 

  15. Vann SD, Brown MW, Erichsen JT, Aggleton JP (2000) Fos imaging reveals differential patterns of hippocampal and parahippocampal subfield activation in rats in response to different spatial memory tests. J Neurosci 20: 2711–2718.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. de Hoz L, Knox J, Morris RG (2003) Longitudinal axis of the hippocampus: both septal and temporal poles of the hippocampus support water maze spatial learning depending on the training protocol. Hippocampus 13: 587–603. https://doi.org/10.1002/hipo.10079

    Article  PubMed  Google Scholar 

  17. Ferbinteanu J, Ray C, McDonald RJ (2003) Both dorsal and ventral hippocampus contribute to spatial learning in Long-Evans rats. Neurosci Lett 345: 131–135.

    Article  CAS  PubMed  Google Scholar 

  18. Dong HW, Swanson LW, Chen L, Fanselow MS, Toga AW (2009) Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc Natl Acad Sci USA 106: 11794–11799.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bienkowski MS, Bowman I, Song MY, et al. (2018) Integration of gene expression and brain-wide connectivity reveals the multiscale organization of mouse hippocampal networks. Nat Neurosci 21: 1628–1643. https://doi.org/10.1038/s41593-018-0241-y

  20. Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA 99: 10825–10830. https://doi.org/10.1073/pnas.152112399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Degroot A, Treit D (2004) Anxiety is functionally segregated within the septo-hippocampal system. Brain Res 1001: 60–71. https://doi.org/10.1016/j.brainres.2003.10.065

    Article  CAS  PubMed  Google Scholar 

  22. Häckl LPN, Carobrez AP (2007) Distinct ventral and dorsal hippocampus AP5 anxiolytic effects revealed in the elevated plus-maze task in rats. Neurobiol Learn Mem 88: 177–185. https://doi.org/10.1016/j.nlm.2007.04.007

    Article  CAS  Google Scholar 

  23. McHugh SB, Deacon RM, Rawlins JN, Bannerman DM (2004) Amygdala and ventral hippocampus contribute differentially to mechanisms of fear and anxiety. Behav Neurosci 118: 63–78. https://doi.org/10.1037/0735-7044.118.1.63

    Article  CAS  PubMed  Google Scholar 

  24. Bannerman DM, Grubb M, Deacon RM, Yee BK, Feldon J, Rawlins JN (2003) Ventral hippocampal lesions affect anxiety but not spatial learning. Behav Brain Res 139: 197–213.

    Article  CAS  PubMed  Google Scholar 

  25. Zhu H, Pleil KE, Urban DJ, Moy SS, Kash TL, Roth BL (2014) Chemogenetic inactivation of ventral hippocampal glutamatergic neurons disrupts consolidation of contextual fear memory. Neuropsychopharmacology 39: 1880–1892. https://doi.org/10.1038/npp.2014.35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Bardgett ME, Henry JD (1999) Locomotor activity and accumbens Fos expression driven by ventral hippocampal stimulation require D1 and D2 receptors. Neuroscience 94: 59–70.

    Article  CAS  PubMed  Google Scholar 

  27. Zhang WN, Bast T, Feldon J (2002) Effects of hippocampal N-methyl-D-aspartate infusion on locomotor activity and prepulse inhibition: differences between the dorsal and ventral hippocampus. Behav Neurosci 116: 72–84. https://doi.org/10.1037//0735-7044.116.1.72

    Article  CAS  PubMed  Google Scholar 

  28. Bast T, Feldon J (2003) Hippocampal modulation of sensorimotor processes. Prog Neurobiol 70: 319–345.

    Article  CAS  PubMed  Google Scholar 

  29. Zornoza T, Cano-Cebrian MJ, Martinez-Garcia F, Polache A, Granero L (2005) Hippocampal dopamine receptors modulate c Fos expression in the rat nucleus accumbens evoked by chemical stimulation of the ventral hippocampus. Neuropharmacology 49: 1067–1076.

    Article  CAS  PubMed  Google Scholar 

  30. Mogenson GJ, Jones DL, Yim CY (1980) From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 14: 69–97. https://doi.org/10.1016/0301-0082(80)90018-0

    Article  CAS  PubMed  Google Scholar 

  31. Swanson LW (1981) A direct projection from Ammon’s horn to prefrontal cortex in the rat. Brain Res 217: 150–154. https://doi.org/10.1016/0006-8993(81)90192-x

    Article  CAS  PubMed  Google Scholar 

  32. 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: 1–26. https://doi.org/10.1016/j.brainresrev.2007.05.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Hok V, Save E, Lenck-Santini PP, Poucet B (2005) Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. Proc Natl Acad Sci USA 102: 4602–4607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Padilla-Coreano N, Bolkan SS, Pierce GM, et al. (2016) Direct ventral hippocampal-prefrontal input is required for anxiety-related neural activity and behavior. Neuron 89: 857–866. https://doi.org/10.1016/j.neuron.2016.01.011

  35. Euston DR, Gruber AJ, McNaughton BL (2012) The role of medial prefrontal cortex in memory and decision making. Neuron 76: 1057–1070. https://doi.org/10.1016/j.neuron.2012.12.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Nadel L, Hoscheidt S, Ryan LR (2013) Spatial cognition and the hippocampus: the anterior-posterior axis. J Cogn Neurosci 25: 22–28. https://doi.org/10.1162/jocn_a_00313

    Article  PubMed  Google Scholar 

  37. McHugh TJ, Blum KI, Tsien JZ, Tonegawa S, Wilson MA (1996) Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell 87: 1339–1349. https://doi.org/10.1016/s0092-8674(00)81828-0

    Article  CAS  PubMed  Google Scholar 

  38. Fenton AA, Kao HY, Neymotin SA, et al. (2008) Unmasking the CA1 ensemble place code by exposures to small and large environments: more place cells and multiple, irregularly arranged, and expanded place fields in the larger space. J Neurosci 28: 11250–11262. https://doi.org/10.1523/JNEUROSCI.2862-08.2008

  39. Park E, Dvorak D, Fenton AA (2011) Ensemble place codes in hippocampus: CA1, CA3, and dentate gyrus place cells have multiple place fields in large environments. PLoS One 6: e22349. https://doi.org/10.1371/journal.pone.0022349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Harland B, Contreras M, Souder M, Fellous JM (2021) Dorsal CA1 hippocampal place cells form a multi-scale representation of megaspace. Curr Biol 31: 2178–2190. e6. https://doi.org/10.1016/j.cub.2021.03.003

    Article  CAS  PubMed  Google Scholar 

  41. Jung MW, Wiener SI, McNaughton BL (1994) Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14: 7347–7356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kjelstrup KB, Solstad T, Brun VH, et al. (2008) Finite scale of spatial representation in the hippocampus. Science 321: 140–143. https://doi.org/10.1126/science.1157086

  43. Royer S, Sirota A, Patel J, Buzsáki G (2010) Distinct representations and theta dynamics in dorsal and ventral hippocampus. J Neurosci 30: 1777–1787. https://doi.org/10.1523/JNEUROSCI.4681-09.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Komorowski RW, Garcia CG, Wilson A, Hattori S, Howard MW, Eichenbaum H (2013) Ventral hippocampal neurons are shaped by experience to represent behaviorally relevant contexts. J Neurosci 33: 8079–8087. https://doi.org/10.1523/jneurosci.5458-12.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Eilam D, Dank M, Maurer R (2003) Voles scale locomotion to the size of the open-field by adjusting the distance between stops: a possible link to path integration. Behav Brain Res 141: 73–81.

    Article  PubMed  Google Scholar 

  46. Whishaw IQ, Gharbawie OA, Clark BJ, Lehmann H (2006) The exploratory behavior of rats in an open environment optimizes security. Behav Brain Res 171: 230–239. https://doi.org/10.1016/j.bbr.2006.03.037

    Article  PubMed  Google Scholar 

  47. Lebedev IV, Pleskacheva MG, Anokhin KV (2012) C57BL/6 mice open field behavior qualitatively depends on arena size. Zh Vyssh Nerv Deiat Im IP Pavlova 62: 485–496.

    CAS  Google Scholar 

  48. Kuptsov PA, Pleskacheva MG, Anokhin KV (2012) Inhomogeneous hippocampal activation along the rostrocaudal axis in mice after exploration of novel environment. Zh Vyssh Nerv Deiat Im IP Pavlova 62: 43–55.

    CAS  Google Scholar 

  49. Kuptsov PA, Pleskacheva MG, Voronkov DN, Lipp H-P, Anokhin KV (2006) Features of the expression of the c-Fos gene along the rostrocaudal axis of the hippocampus in common voles after rapid training to solve a spatial task. Neurosci Behav Physiol 36: 341–350. https://doi.org/10.1007/s11055-006-0023-y

    Article  CAS  PubMed  Google Scholar 

  50. Kuptsov PA (2006) Study of activation of different subregion of rodent hippocampus after spatial task performance. Ph. D. Thesis. Lomonosov Moscow State University: Moscow.

  51. Kuptsov PA, Pleskacheva MG, Anokhin KV (2021) The size of an explored space is reflected differently in the activity of different subregions of the hippocampus along its septotemporal axis. Neurosci Behav Physiol 51: 734–738. https://doi.org/10.1007/s11055-021-01129-8

    Article  CAS  Google Scholar 

  52. Rossi-Arnaud C, Ammassari-Teule M (1992) Modifications of open field and novelty behaviors by hippocampal and amygdaloid lesions in two inbred strains of mice: Lack of strain × lesion interactions. Behav Processes 27: 155–164. https://doi.org/10.1016/0376-6357(92)90171-9

    Article  CAS  PubMed  Google Scholar 

  53. Dillon GM, Qu X, Marcus JN, Dodart JC (2008) Excitotoxic lesions restricted to the dorsal CA1 field of the hippocampus impair spatial memory and extinction learning in C57BL/6 mice. Neurobiol Learn Mem 90: 426–433. https://doi.org/10.1016/j.nlm.2008.05.008

    Article  PubMed  Google Scholar 

  54. Deacon RM, Croucher A, Rawlins JN (2002) Hippocampal cytotoxic lesion effects on species-typical behaviors in mice. Behav Brain Res 132: 203–213.

    Article  PubMed  Google Scholar 

  55. Josey M, Brigman JL (2015) Loss of hippocampal function impairs pattern separation on a mouse touch-screen operant paradigm. Neurobiol Learn Mem 125: 85–92. https://doi.org/10.1016/j.nlm.2015.08.002

    Article  PubMed  PubMed Central  Google Scholar 

  56. Yi JH, Park HJ, Kim BC, Kim DH, Ryu JH (2016) Evidences of the role of the rodent hippocampus in the non-spatial recognition memory. Behav Brain Res 297: 141–149. https://doi.org/10.1016/j.bbr.2015.10.018

    Article  PubMed  Google Scholar 

  57. Wolfer DP, Madani R, Valenti P, Lipp HP (2001) Extended analysis of path data from mutant mice using the public domain software Wintrack. Physiol Behav 73: 745–753.

    Article  CAS  PubMed  Google Scholar 

  58. Paxinos G, Franklin KBJ (2004) The mouse brain in stereotaxic coordinates; Second ed. Academic Press, San Diego.

    Google Scholar 

  59. Nadel L (1968) Dorsal and ventral hippocampal lesions and behavior. Physiol Behav 3: 891–900. https://doi.org/10.1016/0031-9384(68)90174-1

    Article  Google Scholar 

  60. Jarrard LE (1968) Behavior of hippocampal lesioned rats in home cage and novel situations. Physiol Behav 3: 65–70. https://doi.org/10.1016/0031-9384(68)90033-4

    Article  Google Scholar 

  61. Cembrowski MS, Bachman JL, Wang L, Sugino K, Shields BC, Spruston N (2016) Spatial gene-expression gradients underlie prominent heterogeneity of CA1 pyramidal neurons. Neuron 89: 351–368. https://doi.org/10.1016/j.neuron.2015.12.013

    Article  CAS  PubMed  Google Scholar 

  62. Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O’Keefe J (1998) Knowing where and getting there: a human navigation network. Science 280: 921–924. https://doi.org/10.1126/science.280.5365.921

    Article  CAS  PubMed  Google Scholar 

  63. Evensmoen HR, Ladstein J, Hansen TI, et al. (2015) From details to large scale: the representation of environmental positions follows a granularity gradient along the human hippocampal and entorhinal anterior-posterior axis. Hippocampus 25: 119–135. https://doi.org/10.1002/hipo.22357

  64. Gray JA, McNaughton N (1983) Comparison between the behavioral effects of septal and hippocampal lesions: a review. Neurosci Biobehav Rev 7: 119–188. https://doi.org/10.1016/0149-7634(83)90014-3

    Article  CAS  PubMed  Google Scholar 

  65. Roberts WW, Dember WN, Brodwick M (1962) Alternation and exploration in rats with hippocampal lesions. J Compar Physiol Psychol 55: 695–700. https://doi.org/10.1037/h0045168

    Article  CAS  Google Scholar 

  66. Kimble DP (1963) The effects of bilateral hippocampal lesions in rats. J Comp Physiol Psychol 56: 273–283. https://doi.org/10.1037/h0048903

    Article  CAS  PubMed  Google Scholar 

  67. Douglas RJ, Isaacson RL (1964) Hippocampal lesions and activity. Psychon Sci 1: 187–188. https://doi.org/10.3758/bf03342856

    Article  Google Scholar 

  68. Strong PN, Jackson WJ (1970) Effects of hippocampal lesions in rats on three measures of activity. J Comp Physiol Psychol 70: 60–65. https://doi.org/10.1037/h0028391

    Article  PubMed  Google Scholar 

  69. Lanier LP, Isaacson RL (1975) Activity changes related to the location of lesion in the hippocampus. Behav Biol 13: 59–69. https://doi.org/10.1016/s0091-6773(75)90793-2

    Article  CAS  PubMed  Google Scholar 

  70. Whishaw IQ, Jarrard LE (1995) Similarities vs. differences in place learning and circadian activity in rats after fimbria-fornix section or ibotenate removal of hippocampal cells. Hippocampus 5: 595–604.

    Article  CAS  PubMed  Google Scholar 

  71. Good M, Honey RC (1997) Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning. Behav Neurosci 111: 487–493.

    Article  CAS  PubMed  Google Scholar 

  72. Clark BJ, Hines DJ, Hamilton DA, Whishaw IQ (2005) Movements of exploration intact in rats with hippocampal lesions. Behav Brain Res 163: 91–99. https://doi.org/10.1016/j.bbr.2005.04.007

    Article  PubMed  Google Scholar 

  73. Weeden CS, Roberts JM, Kamm AM, Kesner RP (2015) The role of the ventral dentate gyrus in anxiety-based behaviors. Neurobiol Learn Mem 118: 143–149. https://doi.org/10.1016/j.nlm.2014.12.002

    Article  PubMed  Google Scholar 

  74. Teitelbaum H, Milner P (1963) Activity changes following partial hippocampal lesions in rats. J Compar Physiol Psychol 56: 284–289. https://doi.org/10.1037/h0047052

    Article  CAS  Google Scholar 

  75. Bender RM, Hostetter G, Thomas GJ (1968) Effects of lesions in hippocampus-entorhinal cortex on maze performance and activity in rats. journal article. Psychon Sci 10: 13–14. https://doi.org/10.3758/bf03331382

    Article  Google Scholar 

  76. Roberts WW, Dember WN, Brodwick M (1962) Alternation and exploration in rats with hippocampal lesions. J Comp Physiol Psychol 55: 695–700. https://doi.org/10.1037/h0045168

    Article  CAS  PubMed  Google Scholar 

  77. Lipska BK, Jaskiw GE, Chrapusta S, Karoum F, Weinberger DR (1992) Ibotenic acid lesion of the ventral hippocampus differentially affects dopamine and its metabolites in the nucleus accumbens and prefrontal cortex in the rat. Brain Res 585: 1–6.

    Article  CAS  PubMed  Google Scholar 

  78. Moses SN, Sutherland RJ, McDonald RJ (2002) Differential involvement of amygdala and hippocampus in responding to novel objects and contexts. Brain Res Bull 58: 517–527. https://doi.org/10.1016/s0361-9230(02)00820-1

    Article  PubMed  Google Scholar 

  79. Wallace DG, Whishaw IQ (2003) NMDA lesions of Ammon’s horn and the dentate gyrus disrupt the direct and temporally paced homing displayed by rats exploring a novel environment: evidence for a role of the hippocampus in dead reckoning. Eur J Neurosci 18: 513–523.

    Article  PubMed  Google Scholar 

  80. Winter SS, Koppen JR, Ebert TB, Wallace DG (2013) Limbic system structures differentially contribute to exploratory trip organization of the rat. Hippocampus 23: 139–152. https://doi.org/10.1002/hipo.22075

    Article  PubMed  Google Scholar 

  81. Anderson MI, Killing S, Morris C, et al. (2006) Behavioral correlates of the distributed coding of spatial context. Hippocampus 16: 730–742.

  82. Lever C, Burton S, O’Keefe J (2006) Rearing on hind legs, environmental novelty, and the hippocampal formation. Rev Neurosci 17: 111–133.

    Article  PubMed  Google Scholar 

  83. Poulter S, Hartley T, Lever C (2018) The neurobiology of mammalian navigation. Curr Biol 28: R1023–R1042. https://doi.org/10.1016/j.cub.2018.05.050

    Article  CAS  PubMed  Google Scholar 

  84. Crusio WE, Schwegler H, Brust I, Van Abeelen JH (1989) Genetic selection for novelty-induced rearing behavior in mice produces changes in hippocampal mossy fiber distributions. J Neurogenet 5: 87–93.

    Article  CAS  PubMed  Google Scholar 

  85. Wells CE, Amos DP, Jeewajee A, et al. (2013) Novelty and anxiolytic drugs dissociate two components of hippocampal theta in behaving rats. J Neurosci 33: 8650–8667. https://doi.org/10.1523/jneurosci.5040-12.2013

  86. Barth AM, Domonkos A, Fernandez-Ruiz A, Freund TF, Varga V (2018) Hippocampal Network Dynamics during Rearing Episodes. Cell Rep 23: 1706–1715. https://doi.org/10.1016/j.celrep.2018.04.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Harley CW, Martin GM (1999) Open field motor patterns and object marking, but not object sniffing, are altered by ibotenate lesions of the hippocampus. Neurobiol Learn Mem 72: 202–214.

    Article  CAS  PubMed  Google Scholar 

  88. Sturman O, Germain PL, Bohacek J (2018) Exploratory rearing: a context- and stress-sensitive behavior recorded in the open-field test. Stress 21: 443–452. https://doi.org/10.1080/10253890.2018.1438405

    Article  PubMed  Google Scholar 

  89. Deacon RM, Rawlins JN (2005) Hippocampal lesions, species-typical behaviors and anxiety in mice. Behav Brain Res 156: 241–249. https://doi.org/10.1016/j.bbr.2004.05.027

    Article  PubMed  Google Scholar 

  90. Contreras M, Pelc T, Llofriu M, Weitzenfeld A, Fellous JM (2018) The ventral hippocampus is involved in multi-goal obstacle-rich spatial navigation. Hippocampus 28: 853–866. https://doi.org/10.1002/hipo.22993

    Article  PubMed  Google Scholar 

  91. Moser MB, Moser EI (1998) Functional differentiation in the hippocampus. Hippocampus 8: 608–619. https://doi.org/10.1002/(sici)1098-1063(1998)8:6<608::aid-hipo3>3.0.co;2-7

    Article  CAS  PubMed  Google Scholar 

  92. Parfitt GM, Nguyen R, Bang JY, et al. (2017) Bidirectional control of anxiety-related behaviors in mice: role of inputs arising from the ventral hippocampus to the lateral septum and medial prefrontal cortex. Neuropsychopharmacology 42: 1715–1728. https://doi.org/10.1038/npp.2017.56

  93. McHugh TJ, Tonegawa S (2007) Spatial exploration is required for the formation of contextual fear memory. Behav Neurosci 121: 335–339. https://doi.org/10.1037/0735-7044.121.2.335

    Article  PubMed  Google Scholar 

  94. 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. https://doi.org/10.1111/j.1460-9568.2010.07497.x

    Article  PubMed  PubMed Central  Google Scholar 

  95. Hartley T, Maguire EA, Spiers HJ, Burgess N (2003) The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 37: 877–888.

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors are grateful to I.V. Lebedev for his help in carrying out experiments.

Funding

Supported by RFBR 20-015-00287.

The research was carried out within the project of state assignment of MSU No. 121032500080-8.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: Pleskacheva MG, Anokhin KV; Methodology: Deacon RMG, Kuptsov PA; Formal analysis and investigation: Kuptsov PA, Pleskacheva MG; Writing: original draft preparation: Pleskacheva MG, Kuptsov PA; Writing: review and editing: Pleskacheva MG, Deacon RMG, Anokhin KV.

Corresponding author

Correspondence to M. G. Pleskacheva.

Ethics declarations

CONFLICT OF INTEREST

The authors state no conflict of interest with respect to the research, authorship, and/or publication of this article.

SUPPLEMENTARY INFORMATION

The online version contains supplementary material available at 10.1134/S0022093023040099.

10893_2023_8468_MOESM1_ESM.pdf

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kuptsov, P.A., Deacon, R.M.J., Anokhin, K.V. et al. Exploratory and Locomotor Activity in Mice Following Selective Lesions of the Hippocampus: Effects of Lesion Site and Open Field Arena Size. J Evol Biochem Phys 59, 1112–1135 (2023). https://doi.org/10.1134/S0022093023040099

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0022093023040099

Keywords:

Navigation