Spatial working memory activity of the caudate nucleus is sensitive to frame of reference

  • Bradley R. PostleEmail author
  • Mark D’Esposito


We used event-related fMRI to test the hypothesis that the caudate nucleus is preferentially recruited by a spatial working memory task employing egocentrically defined stimuli, which are amenable to transformation into a motor code, as contrasted with allocentrically defined stimuli, which are not. Our results revealed greater delay-epoch activity in egocentric than in allocentric trials in the caudate nucleus and trends in the same direction in the putamen and the lateral premotor cortex (PMC). Response-related activity was greater for egocentric trials in the lateral PMC. We propose that the neostriatum, possibly interacting with the PMC, may contribute to the sensory-motor transformation necessary to establish a prospective motor code (e.g., the representation of a saccade or a grasp). In addition, the PMC may participate in decision-making processes, prompted by the onset of the probe stimulus, that employ this prospective motor information. This model accounts for the empirical evidence that motor distraction disrupts spatial working memory performance.


Caudate Nucleus Work Memory Task Blood Oxygen Level Dependent Visual Working Memory Probe Stimulus 
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  1. Aguirre, G. K., Zarahn, E., & D’Esposito, M. (1998). The variability of human, BOLD hemodynamic responses. NeuroImage, 8, 360–369.PubMedCrossRefGoogle Scholar
  2. Andersen, R. A., Essick, G. K., & Siegel, R. M. (1985). Encoding of spatial location by posterior parietal neurons. Science, 230, 456–458.PubMedCrossRefGoogle Scholar
  3. Ashburner, J., & Friston, K. (1996). Fully three-dimensional nonlinear spatial normalization: A new approach. NeuroImage, 3, S111.CrossRefGoogle Scholar
  4. Awh, E., Anllo-Vento, L., & Hillyard, S. A. (2000). The role of spatial selective attention in working memory for locations: Evidence from event-related potentials. Journal of Cognitive Neuroscience, 12, 840–847.PubMedCrossRefGoogle Scholar
  5. Awh, E., & Jonides, J. (2001). Overlapping mechanisms of attention and spatial working memory. Trends in Cognitive Sciences, 5, 119–126.PubMedCrossRefGoogle Scholar
  6. Awh, E., Jonides, J., & Reuter-Lorenz, P. A. (1998). Rehearsal in spatial working memory. Journal of Experimental Psychology: Human Perception & Performance, 24, 780–790.CrossRefGoogle Scholar
  7. Awh, E., Jonides, J., Smith, E. E., Buxton, R. B., Frank, L. R., Love, T., Wong, E. C., & Gmeindl, L. (1999). Rehearsal in spatial working memory: Evidence from neuroimaging. Psychological Science, 10, 433–437.CrossRefGoogle Scholar
  8. Baddeley, A. D. (1986). Working memory. London: Oxford University Press.Google Scholar
  9. Baddeley, A. D., & Hitch, G. J. (1974). Working memory. In G. H. Bower (Ed.), The psychology of learning and motivation (Vol. 8, pp. 47–89). New York: Academic Press.Google Scholar
  10. Baddeley, A. D., & Lieberman, K. (1980). Spatial working memory. In R. S. Nickerson (Ed.), Attention and performance VIII (pp. 521–539). Hillsdale, NJ: Erlbaum.Google Scholar
  11. Baddeley, A. D., & Logie, R. H. (1999). Working memory: The multiplecomponent model. In A. Miyake & P. Shah (Eds.), Models of working memory (pp. 28–61). Cambridge: Cambridge University Press.Google Scholar
  12. Battig, K., Rosvold, H. E., & Mishkin, M. (1960). Comparison of the effects of frontal and caudate lesions on delayed response and alternation in monkeys. Journal of Comparative & Physiological Psychology, 53, 400–404.CrossRefGoogle Scholar
  13. Boynton, G. M., Engel, S. A., Glover, G. H., & Heeger, D. J. (1996). Linear systems analysis of functional magnetic resonance imaging in human V1. Journal of Neuroscience, 16, 4207–4221.PubMedGoogle Scholar
  14. Brett, M., Johnsrude, I. S., & Owen, A. M. (2002). The problem of functional localization in the human brain. Nature Reviews: Neuroscience, 3, 243–249.PubMedCrossRefGoogle Scholar
  15. Butters, N., Soeldner, C., & Fedio, P. (1972). Comparison of parietal and frontal lobe spatial deficits in man: Extrapersonal vs. personal (egocentric) space. Perceptual & Motor Skills, 34, 27–34.Google Scholar
  16. Cheffi, S., Allport, D. A., & Woodin, M. (1999). Hand-centered coding of target location in visuo-spatial working memory. Neuropsychologia, 37, 495–502.CrossRefGoogle Scholar
  17. Corbetta, M., Kincade, J. M., & Shulman, G. L. (2002). Neural systems for visual orienting and their relationships to spatial working memory. Journal of Cognitive Neuroscience, 14, 508–523.PubMedCrossRefGoogle Scholar
  18. Courtney, S. M., Ungerleider, L. G., Keil, K., & Haxby, J. (1996). Object and spatial visual working memory activate separate neural systems in human cortex. Cerebral Cortex, 6, 39–49.PubMedCrossRefGoogle Scholar
  19. Damasio, H. (1995). Human brain anatomy in computerized images. Oxford: Oxford University Press.Google Scholar
  20. Dean, W. H., & Davis, G. D. (1959). Behavior changes following caudate lesions in rhesus monkey. Journal of Neurophysiology, 22, 525–537.Google Scholar
  21. Della Sala, S., Gray, C., Baddeley, A., Allamano, N., & Wilson, L. (1999). Pattern span: A tool for unwelding visuo-spatial memory. Neuropsychologia, 37, 1189–1199.PubMedCrossRefGoogle Scholar
  22. D’Esposito, M., Aguirre, G. K., Zarahn, E., & Ballard, D. (1998). Functional MRI studies of spatial and non-spatial working memory. Cognitive Brain Research, 7, 1–13.PubMedCrossRefGoogle Scholar
  23. D’Esposito, M., Ballard, D., Aguirre, G. K., & Zarahn, E. (1998). Human prefrontal cortex is not specific for working memory: A functional MRI study. NeuroImage, 8, 274–282.PubMedCrossRefGoogle Scholar
  24. Divac, I., Rosvold, H. E., & Szwarcbart, M. K. (1967). Behavioral effects of selective ablation of the caudate nucleus. Journal of Comparative & Physiological Psychology, 63, 184–190.CrossRefGoogle Scholar
  25. Duvernoi, H. M. (1999). The human brain: Surface, blood supply, and three-dimensional sectional anatomy (2nd ed.). New York: Springer-Verlag.Google Scholar
  26. Farmer, E. W., Berman, J. V. F., & Fletcher, Y. L. (1986). Evidence for a visuo-spatial scratch-pad in working memory. Quarterly Journal of Experimental Psychology, 38A, 675–688.Google Scholar
  27. Friston, K. J., Ashburner, J., Frith, C. D., Poline, J.-B., Heather, J. D., & Frackowiak, R. S. J. (1995). Spatial registration and normalization of images. Human Brain Mapping, 2, 165–189.CrossRefGoogle Scholar
  28. Galati, G., Lobel, E., Berthoz, A., Pizzamiglio, L., Le Bihan, D., & Vallar, G. (1999). Egocentric and allocentric coding of space in the human brain. NeuroImage, 9, S745.Google Scholar
  29. Goldman, P. S., & Rosvold, H. E. (1972). The effects of selective caudate lesions in infant and juvenile rhesus monkeys. Brain Research, 43, 53.PubMedCrossRefGoogle Scholar
  30. Goldman-Rakic, P. S. (1987). Circuitry of the prefrontal cortex and the regulation of behavior by representational memory. In V. B. Mountcastle, F. Plum, & S. R. Geiger (Eds.), Handbook of neurobiology(pp. 373–417). Bethesda, MD: American Physiological Society.Google Scholar
  31. Goldman-Rakic, P. S. (1990). Cellular and circuit basis of working memory in prefrontal cortex of nonhuman primates. In H. B. M. Uylings, C. G. V. Eden, J. P. C. DeBruin, M. A. Corner, & M. G. P. Feenstra (Eds.), Progress in brain research (Vol. 85, pp. 325–336). Amsterdam: Elsevier.Google Scholar
  32. Graziano, M. S. A., Yap, G. S., & Gross, C. G. (1994). Coding of visual space by premotor neurons. Science, 266, 1054–1057.PubMedCrossRefGoogle Scholar
  33. Hale, S., Myerson, J., Rhee, S. H., Weiss, C. S., & Abrams, R. A. (1996). Selective interference with the maintenance of location information in working memory. Neuropsychology, 10, 228–240.CrossRefGoogle Scholar
  34. Kesner, R. P., Bolland, B. L., & Dakis, M. (1993). Memory for spatial locations, motor responses, and objects: Triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Experimental Brain Research, 93, 462–470.CrossRefGoogle Scholar
  35. Lawrence, B. M., Myerson, J., Oonk, H. M., & Abrams, R. A. (2001). The effects of eye and limb movements on working memory. Memory, 9, 433–444.CrossRefGoogle Scholar
  36. Leung, H.-C., Gore, J. C., & Goldman-Rakic, P. S. (2002). Sustained mnemonic response in the human middle frontal gyrus during on-line storage of spatial memoranda. Journal of Cognitive Neuroscience, 14, 659–671.PubMedCrossRefGoogle Scholar
  37. Levy, R., Friedman, H. R., Davachi, L., & Goldman-Rakic, P. S. (1997). Differential activation of the caudate nucleus in primates performing spatial and nonspatial working memory tasks. Journal of Neuroscience, 17, 3870–3882.PubMedGoogle Scholar
  38. Logie, R. H. (1995). Visuo-spatial working memory. Hove, U.K.: Erlbaum.Google Scholar
  39. Logie, R. H., & Marchetti, C. (1991). Visuo-spatial working memory: Visual, spatial or central executive? In R. H. Logie & M. Denis (Eds.), Mental images in human cognition (pp. 105–115). Amsterdam: Elsevier.CrossRefGoogle Scholar
  40. Mai, J. K., Assheuer, J., & Paxinos, G. (1997). Atlas of the human Brain. San Diego: Academic Press.Google Scholar
  41. Owen, A. M., Iddon, J. L., Hodges, J. R., Summers, B. A., & Robbins, T. W. (1997). Spatial and non-spatial working memory at different stages of Parkinson’s disease. Neuropsychologia, 35, 519–532.PubMedCrossRefGoogle Scholar
  42. Pohl, W. (1973). Dissociation of spatial discrimination deficits following frontal and parietal lesions in monkeys. Journal of Comparative & Physiological Psychology, 82, 227–239.CrossRefGoogle Scholar
  43. Postle, B. R., Berger, J. S., Taich, A. M., & D’Esposito, M. (2000). Activity in human frontal cortex associated with spatial working memory and saccadic behavior. Journal of Cognitive Neuroscience, 12 (Suppl. 2), 2–14.PubMedCrossRefGoogle Scholar
  44. Postle, B. R., & D’Esposito, M. (1999a). Dissociation of caudate nucleus activity in spatial and nonspatial working memory: An eventrelated fMRI study. Cognitive Brain Research, 8, 107–115.CrossRefGoogle Scholar
  45. Postle, B. R., & D’Esposito, M. (1999b). “What”-then-“where” in visual working memory: An event-related fMRI study. Journal of Cognitive Neuroscience, 11, 585–597.PubMedCrossRefGoogle Scholar
  46. Postle, B. R., & D’Esposito, M. (2000). Evaluating models of the topographical organization of working memory function in frontal cortex with event-related fMRI. Psychobiology, 28, 132–145.Google Scholar
  47. Postle, B. R., Jonides, J., Smith, E., Corkin, S., & Growdon, J. H. (1997). Spatial, but not object, delayed response is impaired in early Parkinson’s disease. Neuropsychology, 11, 1–9.CrossRefGoogle Scholar
  48. Postle, B. R., Locascio, J. J., Corkin, S., & Growdon, J. H. (1997). The time course of spatial and object visual learning in early Parkinson’s disease. Neuropsychologia, 35, 1413–1422.PubMedCrossRefGoogle Scholar
  49. Postle, B. R., Stern, C. E., Rosen, B. R., & Corkin, S. (2000). An fMRI investigation of cortical contributions to spatial and nonspatial visual working memory. NeuroImage, 11, 409–423.PubMedCrossRefGoogle Scholar
  50. Postle, B. R., Zarahn, E., & D’Esposito, M. (2000). Using eventrelated fMRI to assess delay-period activity during performance of spatial and nonspatial working memory tasks. Brain Research Protocols, 5, 57–66.PubMedCrossRefGoogle Scholar
  51. Potegal, M. (1982). Vestibular and neostriatal contributions to spatial orientation. In M. Potegal (Ed.), Spatial abilities, development and physiological foundation (pp. 361–387). New York: Academic Press.Google Scholar
  52. Quinn, J. G., & Ralston, G. E. (1986). Movement and attention in visual working memory.Quarterly Journal of Experimental Psychology, 38A, 689–703.Google Scholar
  53. Rafal, R., & Robertson, L. (1995). The neurology of visual attention. In M. S. Gazzaniga (Ed.), The cognitive neurosciences (pp. 625–648). Cambridge, MA: MIT Press.Google Scholar
  54. Rajkowska, G., & Goldman-Rakic, P. S. (1995). Cytoarchitectonic definition of prefrontal areas in the normal human cortex: II. Variability in locations of areas 9 and 46 and relationship to the Talairach coordinate system. Cerebral Cortex, 5, 323–337.PubMedCrossRefGoogle Scholar
  55. Rosvold, H. E., & Delgado, J. M. R. (1956). The effect on delayedattention test performance of stimulating or destroying electrically structures within the frontal lobes of the monkey’s brain. Journal of Comparative & Physiological Psychology, 49, 365–372.CrossRefGoogle Scholar
  56. Salway, A. F. S., & Logie, R. H. (1995). Visuospatial working memory, movement control and executive demands. British Journal of Psychology, 86, 253–269.PubMedGoogle Scholar
  57. Semmes, J., Weinstein, S., Ghent, L., & Teuber, H.-L. (1963). Correlates of impaired orientation in personal and extrapersonal space. Brain, 86, 747–772.PubMedCrossRefGoogle Scholar
  58. Smith, E. E., Jonides, J., Koeppe, R. A., Awh, E., Schumacher, E. H., & Minoshima, S. (1995). Spatial vs. object working memory: PET investigations. Journal of Cognitive Neuroscience, 7, 337–356.CrossRefGoogle Scholar
  59. Smyth, M. M., Pearson, N. A., & Pendleton, L. R. (1988). Movement and working memory: Patterns and positions in space. Quarterly Journal of Experimental Psychology, 40A, 497–514.Google Scholar
  60. Snyder, L. H., Grieve, K. L., Brotchie, P., & Andersen, R. A. (1998). Separate body- and world-referenced representations of visual space in parietal cortex. Nature, 394, 887–891.PubMedCrossRefGoogle Scholar
  61. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme.Google Scholar
  62. Tresch, M. C., Sinnamon, H. M., & Seamon, J. G. (1993). Double dissociation of spatial and object visual memory: Evidence from selective interference in intact human subjects. Neuropsychologia, 31, 211–219.PubMedCrossRefGoogle Scholar
  63. Ungerleider, L. G., & Haxby, J. V. (1994). “What” and “where” in the human brain. Current Opinion in Neurobiology, 4, 157–165.PubMedCrossRefGoogle Scholar
  64. Ungerleider, L. G., & Mishkin, M. (1982). Two cortical visual systems. In D. J. Ingle, M. A. Goodale, & R. J. W. Mansfield (Eds.), Analysis of visual behavior (pp. 549–586). Cambridge, MA: MIT Press.Google Scholar
  65. Vallar, G., Lobel, E., Galati, G., Berthoz, A., Pizzamiglio, L., & Le Bihan, D. (1999). A fronto-parietal system for computing the egocentric spatial frame of reference in humans. Experimental Brain Research, 124, 281–286.CrossRefGoogle Scholar
  66. Woodin, M. E., & Allport, A. (1999). Independent reference frames in human spatial memory: Body-centered and environment-centered coding in near and far space. Memory & Cognition, 26, 1109–1116.CrossRefGoogle Scholar
  67. Worsley, K. J., & Friston, K. J. (1995). Analysis of fMRI time-series revisited - again. NeuroImage, 2, 173–182.PubMedCrossRefGoogle Scholar
  68. Zarahn, E., Aguirre, G. K., & D’Esposito, M. (1997). A trial-based experimental design for fMRI. NeuroImage, 6, 122–138.PubMedCrossRefGoogle Scholar
  69. Zarahn, E., Aguirre, G. K., & D’Esposito, M. (1999). Temporal isolation of the neural correlates of spatial mnemonic processing with functional MRI. Cognitive Brain Research, 7, 255–268.PubMedCrossRefGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2003

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of WisconsinMadison
  2. 2.University of CaliforniaBerkeley

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