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Evidence for entorhinal and parietal cortices involvement in path integration in the rat

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Abstract

Rats with lesions of the entorhinal or parietal cortex were tested in a homing task on a circular platform containing food cups and surrounded by curtains. The animals had to leave a refuge, explore the platform to find a hidden piece of food and carry it back to the refuge. Once the rats were proficient at performing the procedural aspects of the task, they were tested in two successive types of trials in which the food pellet was either always located in the central cup (food at center, “FAC” trials) or placed in a randomly chosen cup (food at random, “FAR” trials). Except in the first FAC trials, all groups displayed similar outward paths in FAC and FAR trials, showing that both types of trials involved equivalent path integration demand. Analysis of the homing accuracy showed that rats with entorhinal cortex or parietal cortex lesions exhibited inaccurate returns to the starting hole, suggesting that these two cortical areas are part of a neural network mediating path integration.

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References

  • Alyan S, McNaughton BL (1999) Hippocampectomized rats are capable of homing by path integration. Behav Neurosci 113:19–31

    Article  CAS  PubMed  Google Scholar 

  • Batschelet E (1981) Circular statistics in biology. Academic Press, New York

  • Barlow JS (1964) Inertial navigation as a basis for animal navigation. J Theor Biol 6:76–117

    CAS  PubMed  Google Scholar 

  • Benhamou S (1997) Path integration by swimming rats. Anim Behav 54:321–327

    Article  PubMed  Google Scholar 

  • Biegler R (2000) Possible uses of path integration in animal navigation. Anim Learn Behav 28:257–277

    Google Scholar 

  • Burwell RD, Amaral DG (1998) Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. J Comp Neurol 398:179–205

    Article  CAS  PubMed  Google Scholar 

  • Cooper BG, Manka TF, Mizumori SJY (2001) Finding your way in the dark: the retrosplenial cortex contributes to spatial memory and navigation without visual cues. Behav Neurosci 115:1012–1028

    Article  CAS  PubMed  Google Scholar 

  • Etienne AS (1980) The orientation of the golden hamster to its nest-site after the elimination of various sensory cues. Experientia 36:1048–1050

    CAS  PubMed  Google Scholar 

  • Etienne A, Maurer R, Séguinot V (1996) Path integration in mammals and its interaction with visual landmarks. J Exp Biol 199:201–209

    PubMed  Google Scholar 

  • Foreman N, Ermakova I (1998) The radial arm maze: twenty years on. In: Foreman N, Gillett R (eds) Handbook of spatial research paradigms and methodologies, vol 2, clinical and comparative studies. Psychology Press, Hove (UK), pp 87–143

  • Fukushima K (1997) Corticovestibular interactions: anatomy, electrophysiology, and functional considerations. Exp Brain Res 117:1–16

    CAS  PubMed  Google Scholar 

  • Gallistel CR (1990) The organization of learning. MIT Press, Cambridge

  • Golob EJ, Taube JS (1999) Head direction cells in rats with hippocampal or overlying neocortical lesions: evidence for impaired angular path integration. J Neurosci 19:7198–7211

    CAS  PubMed  Google Scholar 

  • Gothard KM, Skaggs WE, McNaughton BL (1996) Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J Neurosci 16:8027–8040

    CAS  PubMed  Google Scholar 

  • Gothard KM, Hoffman KL, Battaglia FP, McNaughton BL (2001) Dentate gyrus and CA1 ensemble activity during spatial reference frame shifts in the presence and absence of visual input. J Neurosci 21:7284–7292

    CAS  PubMed  Google Scholar 

  • Kolb B, Walkey J (1987) Behavioral and anatomical studies of the posterior parietal cortex in the rat. Behav Brain Res 23:127–145

    Article  CAS  PubMed  Google Scholar 

  • Krieg WJS (1946) Connections of the cerebral cortex. 1. The albino rat. A. Topography of the cortical areas. J Comp Neurol 84:221–275

    Google Scholar 

  • Maaswinkel H, Whishaw IQ (1999) Homing with locale, taxon, and dead reckoning strategies by foraging rats: sensory hierarchy in spatial navigation. Behav Brain Res 99:143–152

    Article  CAS  PubMed  Google Scholar 

  • Maaswinkel H, Jarrard LE, Whishaw IQ (1999) Hippocampectomized rats are impaired in homing by path integration. Hippocampus 9:553–561

    Article  CAS  PubMed  Google Scholar 

  • Mittelstaedt H, Mittelstaedt ML (1980) Homing by path integration in a mammal. Naturwissenschaften 67:566

    Google Scholar 

  • Morris RGM (1981) Spatial localization does not require the presence of local cues. Learn Motiv 12:239–260

    Google Scholar 

  • Nishiike S, Guldin W, Bäurle J (2000) Corticofugal connections between the cerebral cortex and the vestibular nuclei in the rat. J Comp Neurol 420:363–372

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G, Watson C (1986) The brain in stereotaxic coordinates. Academic Press, New York

  • Potegal M (1982) Vestibular and neostriatal contributions to spatial orientation. In: Potegal M (ed) Spatial abilities: development and physiological foundations. Academic Press, New York, pp 361–387

  • Potegal M (1987) The vestibular navigation hypothesis: a progress report. In: Ellen P, Thinus-Blanc C (eds) Cognitive processes and spatial orientation in animals and man II Nato ASI Series. Martinus Nijhoff, Dordrecht, pp 28–34

  • Reep RL, Chandler HC, King V, Corwin JV (1994) Rat posterior parietal cortex: topography of corticocortical and thalamic connections. Exp Brain Res 100:67–84

    CAS  PubMed  Google Scholar 

  • Save E, Moghaddam M (1996) Effects of lesions of the associative parietal cortex in the acquisition and use of spatial memory in egocentric and allocentric navigation tasks in the rat. Behav Neurosci 110:74–85

    Article  CAS  PubMed  Google Scholar 

  • Save E, Guazzelli A, Poucet B (2001) Dissociation of the effects of lesions of the dorsal hippocampus and parietal cortex on path integration in the rat. Behav Neurosci 115:1212–1223

    Article  CAS  PubMed  Google Scholar 

  • Sharp P (1999) Complementary roles for hippocampal versus subicular/entorhinal place cells in coding space, context and events. Hippocampus 9:432–443

    Article  CAS  PubMed  Google Scholar 

  • Sharp PE, Blair HT, Etkin D, Tzanetos DB (1995) Influences of vestibular and visual motion information on the spatial firing pattern of hippocampal place cells. J Neurosci 15:173–189

    CAS  PubMed  Google Scholar 

  • Smith PF (1997) Vestibular-hippocampal interactions. Hippocampus 7:465–471

    Article  CAS  PubMed  Google Scholar 

  • Taube JS, Goodridge JP, Golob EJ, Dudchenko PA, Stackman RW (1996) Processing the head direction cell signal: a review and commentary. Brain Res Bull 40:477–486

    Article  CAS  PubMed  Google Scholar 

  • Walker JA, Olton DS (1979) Spatial memory following fimbria-fornix lesions: independent of time for stimulus processing. Physiol Behav 23:11–15

    Article  Google Scholar 

  • Whishaw IQ (1998) Place learning in hippocampal rats and the path integration hypothesis. Neurosci Biobehav Rev 22:209–220

    Article  CAS  PubMed  Google Scholar 

  • Whishaw IQ, Brooks BL (1999) Calibrating space: exploration is important for allothetic and idiothetic navigation. Hippocampus 9:659–667

    Article  CAS  PubMed  Google Scholar 

  • Whishaw IQ, Gorny B (1999) Path integration absent in scent-tracking fimbria-fornix rats: evidence for hippocampal involvement in “sense of direction” and “sense of distance” using self-movement cues. J Neurosci 19:4662–4673

    CAS  PubMed  Google Scholar 

  • Whishaw IQ, Jarrard LE (1996) Evidence for extrahippocampal involvement in place learning and hippocampal involvement in path integration. Hippocampus 6:513–524

    Article  CAS  PubMed  Google Scholar 

  • Whishaw IQ, Maaswinkel H (1998) Rats with fimbria-fornix lesions are impaired in path integration; a role for the hippocampus in “sense of direction”. J Neurosci 18:3050–3058

    CAS  PubMed  Google Scholar 

  • Whishaw IQ, Tomie J-A (1997) Piloting and dead reckoning dissociated by fimbria-fornix lesions in a rat food carrying task. Behav Brain Res 89:87–97

    Article  CAS  PubMed  Google Scholar 

  • Whishaw IQ, Maaswinkel H, Gonzalez CLR, Kolb B (2001) Deficits in allothetic and idiothetic spatial behavior in rats with posterior cingulate cortex lesions. Behav Brain Res 118:67–76

    Article  CAS  PubMed  Google Scholar 

  • Wiener SI, Korshunov VA, Garcia R, Berthoz A (1995) Inertial substratal and landmark cue control of hippocampal CA1 place cell activity. Eur J Neurosci 7:2206–2219

    CAS  PubMed  Google Scholar 

  • Zilles K (1985) The cortex of the rat: a stereotaxic atlas. Springer-Verlag, Berlin

    Google Scholar 

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Acknowledgements

This research was supported by a grant from the French Ministry of Education and Research. We thank B. Poucet for stimulating discussion, H. Lucchessi for histological work, and two anonymous referees for their insightful comments.

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Correspondence to Etienne Save.

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Parron, C., Save, E. Evidence for entorhinal and parietal cortices involvement in path integration in the rat. Exp Brain Res 159, 349–359 (2004). https://doi.org/10.1007/s00221-004-1960-8

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  • DOI: https://doi.org/10.1007/s00221-004-1960-8

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