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Brain activation during human navigation: gender-different neural networks as substrate of performance

Abstract

Visuospatial navigation in animals and human subjects is generally studied using maze exploration. We used functional MRI to observe brain activation in male and female subjects as they searched for the way out of a complex, three-dimensional, virtual-reality maze. Navigation activated the medial occipital gyri, lateral and medial parietal regions, posterior cingulate and parahippocampal gyri as well as the right hippocampus proper. Gender-specific group analysis revealed distinct activation of the left hippocampus in males, whereas females consistently recruited right parietal and right prefrontal cortex. Thus we demonstrate a neural substrate of well established human gender differences in spatial-cognition performance.

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Figure 1: The maze protocol.
Figure 2: Activity of the right hippocampal region in sagittal and transverse planes.
Figure 3: Results of group comparisons superimposed on sagittal and transverse planes.

References

  1. Astur, R. S., Ortiz, M. L. & Sutherland, R. J. A characterization of performance by men and women in a virtual Morris water task: a large and reliable sex difference. Behav. Brain. Res. 93, 185–190 (1998).

    Article  CAS  Google Scholar 

  2. Moffat, E., Hampson, E. & Hatzipantelis, M. Navigation in a ‘virtual’ maze: sex differences and correlation with psychometric measures of spatial ability in humans. Evol. Hum. Behav. 19, 73–87 (1998).

    Article  Google Scholar 

  3. Milner, B. Visually-guided maze learning in man: effects of bilateral hippocampal, bilateral frontal, and unilateral cerebral lesions. Neuropsychologia 3, 317–338 (1965).

    Article  Google Scholar 

  4. Pigott, S. & Milner, B. Memory for different aspects of complex visual scenes after unilateral temporal- or frontal-lobe resection. Neuropsychologia 31, 1–15 (1993).

    Article  CAS  Google Scholar 

  5. Smith, M. L. & Milner, B. The role of the right hippocampus in the recall of spatial location. Neuropsychologia 19, 781–793 (1981).

    Article  CAS  Google Scholar 

  6. Petrides, M. Deficits on conditional associative-learning tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia 23, 601–614 (1985).

    Article  CAS  Google Scholar 

  7. Nunn, J. A., Graydon, F. J., Polkey, C. E. & Morris, R. G. Differential spatial memory impairment after right temporal lobectomy demonstrated using temporal titration. Brain 122, 47–59 (1999).

    Article  Google Scholar 

  8. Burgess, N., Jeffery, K. J. & O'Keefe, J. in The Hippocampal and Parietal Foundations of Spatial Cognition (eds. Burgess, N., Jeffery, K. J. & O'Keefe, J.) 3–29 (Oxford Univ. Press, Oxford, 1999).

    Google Scholar 

  9. Corsi, P. M. Human Memory and the Medial Temporal Region of the Brain. Thesis, McGill Univ. (1972).

    Google Scholar 

  10. O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain. Res. 34, 171–175 (1971).

    Article  CAS  Google Scholar 

  11. Muller, R. U., Kubie, J. L. & Ranck, J. B. J. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935–1950 (1987).

    Article  CAS  Google Scholar 

  12. Rolls, E. T. A theory of hippocampal function in memory. Hippocampus 6, 601–620 (1996).

    Article  CAS  Google Scholar 

  13. Feigenbaum, J. D. & Rolls, E. T. Allocentric and egocentric information processing in the hippocampal formation of the behaving primate. Psychobiology 19, 21–40 (1991).

    Google Scholar 

  14. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon, Oxford, 1978).

    Google Scholar 

  15. Thier, P. & Andersen, R. A. Electrical microstimulation suggests two different forms of representation of head-centered space in the intraparietal sulcus of rhesus monkeys. Proc. Natl. Acad. Sci. USA 93, 4962–4967 (1996).

    Article  CAS  Google Scholar 

  16. Seltzer, B. & Pandya, D. N. Further observations on parieto-temporal connections in the rhesus monkey. Exp. Brain Res. 55, 301–312 (1984).

    Article  CAS  Google Scholar 

  17. Suzuki, W. A. & Amaral, D. G. Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J. Comp. Neurol. 350, 497–533 (1994).

    Article  CAS  Google Scholar 

  18. Goldman-Rakic, P. S. Cellular basis of working memory. Neuron 14, 477–485 (1995).

    Article  CAS  Google Scholar 

  19. Owen, A. M., Evans, A. C. & Petrides, M. Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. Cereb. Cortex 6, 31–38 (1996).

    Article  CAS  Google Scholar 

  20. Salmon, E. et al. Regional brain activity during working memory tasks. Brain 119, 1617–1625 (1996).

    Article  Google Scholar 

  21. Porteus, S. D. Mental tests for the feebleminded: a new series. J. Psycho-Asthenics 12, 200–213 (1915).

    Google Scholar 

  22. Porteus, S. D. The Maze Test and Clinical Psychology (Pacific, Palo Alto, 1959).

    Book  Google Scholar 

  23. Berthoz, A. Parietal and hippocampal contribution to topokinetic and topographic memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 352, 1437–1448 (1997).

    Article  CAS  Google Scholar 

  24. Flitman, S., O'Grady, J., Cooper, V. & Grafman, J. PET imaging of maze processing. Neuropsychologia 35, 409–420 (1997).

    Article  CAS  Google Scholar 

  25. Ghaem, O. et al. Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. Neuroreport 8, 739–744 (1997).

    Article  CAS  Google Scholar 

  26. Van Horn, J. D. et al. Changing patterns of brain activation during maze learning. Brain. Res. 793, 29–38 (1998).

    Article  CAS  Google Scholar 

  27. Maguire, E. A., Frackowiak, R. S. & Frith, C. D. Learning to find your way: a role for the human hippocampal formation. Proc. R. Soc. Lond. B Biol. Sci. 263, 1745–1750 (1996).

    Article  CAS  Google Scholar 

  28. Maguire, E. A., Frackowiak, R. S. J. & Frith, C. D. Recalling routes around London: activation of the right hippocampus in taxi drivers. J. Neurosci. 17, 7103–7110 (1997).

    Article  CAS  Google Scholar 

  29. Aguirre, G. K., Detre, J. A., Alsop, D. C. & D'Esposito, M. The parahippocampus subserves topographical learning in man. Cereb. Cortex 6, 823–829 (1996).

    Article  CAS  Google Scholar 

  30. Maguire, E. A., Frith, C. D., Burgess, N., Donnett, J. G. & O'Keefe, J. Knowing where things are parahippocampal involvement in encoding object locations in virtual large-scale space. J. Cogn. Neurosci. 10, 61–76 (1998).

    Article  CAS  Google Scholar 

  31. Maguire, E. A. et al. Knowing where and getting there: a human navigation network. Science 280, 921–924 (1998).

    Article  CAS  Google Scholar 

  32. Kolb, B. & Cioe, J. Sex-related differences in cortical function after medial frontal lesions in rats. Behav. Neurosci. 110, 1271–1281 (1996).

    Article  CAS  Google Scholar 

  33. Roof, R. L., Zhang, Q., Glasier, M. M. & Stein, D. G. Gender-specific impairment on Morris water maze task after entorhinal cortex lesion. Behav. Brain. Res. 57, 47–51 (1993).

    Article  CAS  Google Scholar 

  34. Maguire, E. A. in The Hippocampal and Parietal Foundations of Spatial Cognition (eds. Burgess, N., Jeffery, K. J. & O'Keefe, J.) 404–415 (Oxford Univ. Press, Oxford, 1999).

    Google Scholar 

  35. Epstein, R., Harris, A., Stanley, D. & Kanwisher, N. The parahippocampal place area: recognition, navigation, or encoding? Neuron 23, 115–125 (1999).

    Article  CAS  Google Scholar 

  36. Colby, C. L. in The Hippocampal and Parietal Foundations of Spatial Cognition (eds. Burgess, N., Jeffery, K. J. & O'Keefe, J.) 104–126 (Oxford Univ. Press, Oxford, 1999).

    Google Scholar 

  37. Shallice, T. et al. Brain regions associated with acquisition and retrieval of verbal episodic memory. Nature 368, 633–635 (1994).

    Article  CAS  Google Scholar 

  38. Fletcher, P. C. et al. Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans. Brain 118, 401–416 (1995).

    Article  Google Scholar 

  39. Fletcher, P. C., Shallice, T., Frith, C. D., Frackowiak, R. S. & Dolan, R. J. Brain activity during memory retrieval. The influence of imagery and semantic cueing. Brain 119, 1587–1596 (1996).

    Article  Google Scholar 

  40. Roland, P. E. & Gulyas, B. Visual memory, visual imagery, and visual recognition of large field patterns by the human brain: functional anatomy by positron emission tomography. Cereb. Cortex 5, 79–93 (1995).

    Article  CAS  Google Scholar 

  41. Cabeza, R. et al. Brain regions differentially involved in remembering what and when: a PET study. Neuron 19, 863–870 (1997).

    Article  CAS  Google Scholar 

  42. Mishkin, M., Ungerleider, L. G. & Macko, K. A. Object vision and spatial vision: two cortical pathways. Trends Neurosci. 6, 414–417 (1983).

    Article  Google Scholar 

  43. Sandstrom, N. J., Kaufman, J. & Huettel, S. A. Males and females use different distal cues in a virtual environment navigation task. Brain. Res. Cogn. Brain Res. 6, 351–360 (1998).

    Article  CAS  Google Scholar 

  44. Vargha-Khadem, F. et al. Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376–380 (1997).

    Article  CAS  Google Scholar 

  45. Strange, B. A., Fletcher, C., Henson, R. N., Friston, K. J. & Dolan, R. J. Segregating the functions of human hippocampus. Proc. Natl. Acad. Sci. USA 96, 4034–4039 (1999).

    Article  CAS  Google Scholar 

  46. Eichenbaum, H., Dudchenko, P., Wood, E., Shapiro, M. & Tanila, H. The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron 23, 209–226 (1999).

    Article  CAS  Google Scholar 

  47. Oldfield, R. C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113 (1971).

    Article  CAS  Google Scholar 

  48. Talairach, J. & Tournoux, P. Co-planar Stereotaxic Atlas of the Human Brain (Thieme, Stuttgart, 1988).

    Google Scholar 

  49. Brodmann, K. Vergleichende Lokalisationslehre der Groβhirnrinde (Barth, Leipzig, 1909).

    Google Scholar 

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Correspondence to Matthias W. Riepe.

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Grön, G., Wunderlich, A., Spitzer, M. et al. Brain activation during human navigation: gender-different neural networks as substrate of performance. Nat Neurosci 3, 404–408 (2000). https://doi.org/10.1038/73980

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