Advertisement

Applied Psychophysiology and Biofeedback

, Volume 30, Issue 3, pp 307–317 | Cite as

fMRI Hippocampal Activity During a VirtualRadial Arm Maze

  • Robert S. Astur
  • Sarah A. St. Germain
  • Elizabeth K. Baker
  • Vince Calhoun
  • Godfrey D. Pearlson
  • R. Todd Constable
Article

Abstract

Numerous studies have shown that the hippocampus is critical for spatial memory. Within nonhuman research, a task often used to assess spatial memory is the radial arm maze. Because of the spatial nature of this task, this maze is often used to assess the function of the hippocampus. Our goal was to extrapolate this task to humans and examine whether healthy undergraduates utilize their hippocampus while performing a virtual reality version of the radial arm maze task. Thirteen undergraduates performed a virtual radial arm maze during functional magnetic resonance imaging. The brain maps of activity reveal bilateral hippocampal BOLD signal changes during the performance of this task. However, paradoxically, this BOLD signal change decreases during the spatial memory component of the task. Additionally, we note frontal cortex activity reflective of working memory circuits. These data reveal that, as predicted by the rodent literature, the hippocampus is involved in performing the virtual radial arm maze in humans. Hence, this virtual reality version may be used to assess the integrity of hippocampus so as to predict risk or severity in a variety of psychiatric disorders.

Keywords

fMRI (functional magnetic resonance imaging) radial arm maze memory hippocampus virtual reality 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aguirre, G. K., Detre, J. A., et al. (1996). The parahippocampus subserves topographical learning in man. Cerebral Cortex, 6(6), 823–829.PubMedGoogle Scholar
  2. Alvarado, M. C., & Rudy, J. W. (1995). Rats with damage to the hippocampal-formation are impaired on the transverse-patterning problem but not on elemental discriminations. Behavioral Neuroscience, 109(2), 204–211.CrossRefPubMedGoogle Scholar
  3. Astur, R. S., St. Germain, S., Mathalon, D. H., D’Souza, D. C., Krystal, J. H., Constable, R. T., et al. (2004). Using virtual reality to investigate the functioning of the hippocampus in schizophrenia (Vol. 1, p. 62). Cybertherapy Abstracts.Google Scholar
  4. Astur, R. S., Tropp, J., et al. (2004). Sex differences and correlations in a virtual Morris water task, a virtual radial arm maze, and mental rotation. Behavioural Brain Research, 151(1–2), 103–115.Google Scholar
  5. Baker, E. K., Demireva, P., et al. (2005). Virtual navigation in individuals with Alzheimer’s disease. New York: Cognitive Neuroscience Society.Google Scholar
  6. Bingman, V. (1988). Unimpaired acquisition of spatial reference memory, but impaired homing performance in hippocampal ablated pigeons. Behavioral Brain Research, 27, 179–188.CrossRefGoogle Scholar
  7. Braak, H., & Braak, E. (1990). Cognitive impairment in Parkinson’s disease: Amyloid plaques, neurofibrillary tangles, and neuropil threads in the cerebral cortex. Journal of Neural Transmission Parkinsons Disease and Dementia Section, 2(1), 45–57.Google Scholar
  8. Bremner, J. D., Randall, P., et al. (1997). Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse—a preliminary report. Biological Psychiatry, 41(1), 23–32.CrossRefPubMedGoogle Scholar
  9. Bunsey, M., & Eichenbaum, H. (1996). Conservation of hippocampal memory function in rats and humans. Nature, 379(6562), 255–257.CrossRefPubMedGoogle Scholar
  10. Cameron, K. A., Yashar, S., et al. (2001). Human hippocampal neurons predict how well word pairs will be remembered. Neuron, 30(1), 289–298.CrossRefPubMedGoogle Scholar
  11. Cohen, N. J., & Eichenbaum, H. (1993). Memory, amnesia, and the hippocampal system (Vol. XII, 330 pp). Cambridge, MA: MIT Press.Google Scholar
  12. Ekstrom, A. D., Kahana, M. J., et al. (2003). Cellular networks underlying human spatial navigation. Nature, 425(6954), 184–187.CrossRefPubMedGoogle Scholar
  13. Freund, T. F., & Buzaki, G. (1996). Interneurons in the hippocampus. Hippocampus, 6, 347–470.CrossRefPubMedGoogle Scholar
  14. Frisk, V., & Milner, B. (1990). The role of the left hippocampal region in the acquisition and retention of story content. Neuropsychologia, 28, 349–359.CrossRefPubMedGoogle Scholar
  15. Groen, G., Wunderlich, A. P., et al. (2000). Brain activation during human navigation: Gender-different neural networks as substrate of performance. Nature Neuroscience, 3(4), 404–408.CrossRefPubMedGoogle Scholar
  16. Hasselmo, M. E., & Wyble, B. P. (1997). Free recall and recognition in a network model of the hippocampus: Simulating effects of scopolamine on human memory function. Behavioural Brain Research, 89(1–2), 1–34.Google Scholar
  17. Huettel, S. A., McKeown, M. J., et al. (2004). Linking hemodynamic and electrophysiological measures of brain activity: Evidence from functional MRI and intracranial field potentials. Cerebral Cortex, 14(2), 165–173.CrossRefPubMedGoogle Scholar
  18. Jones-Gotman, M. (1986). Memory for designs: The hippocampal contribution. Neuropsychologia, 24(2), 193–203.CrossRefPubMedGoogle Scholar
  19. Jones-Gotman, M., Zatorre, R., et al. (1997). Learning and retention of words and designs following excision from medial or lateral temporal-lobe structures. Neuropsychologia, 35(7), 963–973.CrossRefPubMedGoogle Scholar
  20. Kahana, M. J., Sekuler, R., et al. (1999). Human theta oscillations exhibit task dependence during virtual maze navigation. Nature, 399(6738), 781–784.CrossRefPubMedGoogle Scholar
  21. Kandel, E. R., Schwartz, J. H., et al. (1995). Essentials of neural science and behavior. Stamford, UK: Appleton & Lange.Google Scholar
  22. Kim, J. J., & Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear. Science, 256(5057), 675–677.PubMedGoogle Scholar
  23. Lauritzen, M. (2001). Relationship of spikes, synaptic activity, and local changes of cerebral blood flow. Journal of Cerebral Blood Flow and Metabolism, 21(12), 1367–1383.PubMedGoogle Scholar
  24. Logothetis, N. K., Pauls, J., et al. (2001). Neurophysiological investigation of the basis of the fMRI signal [see comment]. Nature, 412(6843), 150–157.CrossRefPubMedGoogle Scholar
  25. Maguire, E. A., Burgess, N., et al. (1998). Knowing where and getting there: A human navigation network. Science, 280(5365), 921–924.CrossRefPubMedGoogle Scholar
  26. Maguire, E. A., Frith, C. D., et al. (1998). Knowing where things are: Parahippocampal involvement in encoding object relations in virtual large-scale space. Journal of Cognitive Neuroscience, 10(1), 61–76.CrossRefPubMedGoogle Scholar
  27. Martin, A. (1999). Automatic activation of the medial temporal lobe during encoding: Lateralized influences of meaning and novelty. Hippocampus, 9(1), 62–70.CrossRefPubMedGoogle Scholar
  28. Milner, B. (1965). Memory disturbances after bilateral hippocampal lesions. In P. Milner & S. Glickman (Eds.), Cognitive processes and the brain. Princeton, NJ: D. Van Nostrand.Google Scholar
  29. Montaldi, D., Mayes, A. R., et al. (1998). Associative encoding of pictures activates the medial temporal lobes. Human Brain Mapping, 6(2), 85–104.CrossRefPubMedGoogle Scholar
  30. Morris, R. G., Garrud, P., et al. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297(5868), 681–683.Google Scholar
  31. Mumby, D. G., Astur, R. S., et al. (1999). Retrograde amnesia and selective damage to the hippocampal formation: Memory for places and object discriminations. Behavioral Brain Research, 106(1–2), 97–107.Google Scholar
  32. O’Keefe, J., & Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Research, 34(1), 171–175.CrossRefPubMedGoogle Scholar
  33. O’Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Clarendon.Google Scholar
  34. Olton, D., Becker, J., et al. (1979). Hippocampus, sapce, and memory. Behavioral and Brain Sciences, 2, 313–366.Google Scholar
  35. Rudy, J. W., & Sutherland, R. J. (1995). Configural association theory and the hippocampal formation: An appraisal and reconfiguration. Hippocampus, 5(5), 375–389.CrossRefPubMedGoogle Scholar
  36. Sanchez-Arroyos, R., Gaztelu, J. M., et al. (1993). Hippocampal and entorhinal glucose metabolism in relation to cholinergic theta rhythm. Brain Research Bulletin, 32(2), 171–178.CrossRefPubMedGoogle Scholar
  37. Scoville, W. B., & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neuropsychiatry and Clinical Neurosciences, 12(1), 103–113.Google Scholar
  38. Sejnowski, T. J., Koch, C., et al. (1990). Computational neuroscience. In S. J. Hanson & C. R. Olson (Eds.), Connectionist modeling and brain function: The developing interface. Neural network modeling and connectionism (pp. 5–35). Cambridge, MA: MIT Press.Google Scholar
  39. Shelton, A. L., & Gabrieli, J. D. E. (2004). Neural correlates of individual differences in spatial learning strategies. Neuropsychology, 18(3), 442–449.CrossRefPubMedGoogle Scholar
  40. Sherry, D. F., Jacobs, L. F., & Gualin, S. J. C. (1992). Spatial memory and adaptive specialization fo the hippocampus. Trends in Neurosciences, 15(8), 298–303.CrossRefPubMedGoogle Scholar
  41. Stern, C. E., & Hasselmo, M. E. (1999). Bridging the gap: Integrating cellular and functional magnetic resonance imaging studies of the hippocampus. Hippocampus, 9(1), 45–53.CrossRefPubMedGoogle Scholar
  42. St. Germain, S. A., Stevens, M., et al. (2004). Virtual navigation in patients with postraumatic stress disorder. San Francisco, CA: Society for Neuroscience.Google Scholar
  43. Taylor, L. B. (1969). Localization of cerebral lesions by psychological testing. Clinical Neurosurgery, 16, 269–287.PubMedGoogle Scholar
  44. Uecker, A., Barnes, C. A., et al. (1997). Hippocampal glycogen metabolism, EEG, and behavior. Behavioral Neuroscience, 111(2), 283–291.CrossRefPubMedGoogle Scholar
  45. Velakoulis, D., Stuart, G. W., et al. (2001). Selective bilateral hippocampal volume loss in chronic schizophrenia. Biological Psychiatry, 50(7), 531–539.CrossRefPubMedGoogle Scholar
  46. Waldvogel, D., van Gelderen, P., et al. (2000). The variability of serial fMRI data: Correlation between a visual and a motor task. Neuroreport: For Rapid Communication of Neuroscience Research, 11(17), 3843–3847.Google Scholar
  47. Walker, J. A., & Olton, D. S. (1979). Spatial memory deficit following fimbria-fornix lesions: Independent of time for stimulus processing. Physiology and Behavior, 23(1), 11–15.CrossRefPubMedGoogle Scholar
  48. Wiebe, S. P., & Staeubli, U. V. (2001). Recognition memory correlates of hippocampal theta cells. Journal of Neuroscience, 21(11), 3955–3967.PubMedGoogle Scholar
  49. Wood, E. R., Dudchenko, P. A., et al. (1999). The global record of memory in hippocampal neuronal activity [see comment]. Nature, 397(6720), 613–616.CrossRefPubMedGoogle Scholar
  50. Zola-Morgan, S., & Squire, L. R. (1990). The neuropsychology of memory: Parallel findings in humans and nonhuman primates. Annals of the New York Academy of Sciences, 608, 434–456.PubMedGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Robert S. Astur
    • 1
    • 2
  • Sarah A. St. Germain
    • 1
  • Elizabeth K. Baker
    • 1
  • Vince Calhoun
    • 1
    • 2
  • Godfrey D. Pearlson
    • 1
    • 2
  • R. Todd Constable
    • 3
    • 4
  1. 1.Olin Neuropsychiatry Research CenterInstitute of LivingHartford
  2. 2.Department of PsychiatryYale School of MedicineNew Haven
  3. 3.Department of Diagnostic RadiologyYale School of MedicineNew Haven
  4. 4.Department of NeurosurgeryYale School of MedicineNew Haven

Personalised recommendations