Imagery neurons in the human brain

Article metrics

Abstract

Vivid visual images can be voluntarily generated in our minds in the absence of simultaneous visual input. While trying to count the number of flowers in Van Gogh's Sunflowers, understanding a description or recalling a path, subjects report forming an image in their “mind's eye”1. Whether this process is accomplished by the same neuronal mechanisms as visual perception has long been a matter of debate1,2,3. Evidence from functional imaging1,4,5,6,7,8, psychophysics1,9, neurological studies2 and monkey electrophysiology10,11,12 suggests a common process, yet there are patients with deficits in one but not the other3,13. Here we directly investigated the neuronal substrates of visual recall by recording from single neurons in the human medial temporal lobe14,15 while the subjects were asked to imagine previously viewed images. We found single neurons in the hippocampus, amygdala, entorhinal cortex and parahippocampal gyrus that selectively altered their firing rates depending on the stimulus the subjects were imagining. Of the neurons that fired selectively during both vision and imagery, the majority (88%) had identical selectivity. Our study reveals single neuron correlates of volitional visual imagery in humans and suggests a common substrate for the processing of incoming visual information and visual recall.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Individual responses of a single neuron during vision and imagery.
Figure 2: Responses of the same neuron as in Fig. 1 during vision and visual imagery.
Figure 3: Responses of a selective neuron in the left amygdala of a different subject during vision and visual imagery.
Figure 4: Comparison of firing rates and Pe between vision and imagery.

References

  1. 1

    Kosslyn, S. M. Image and Brain (MIT Press, Cambridge, 1994).

  2. 2

    Farah, M. J. Is visual imagery really visual? Overlooked evidence from neuropsychology. Psychol. Rev. 95, 307–317 (1988).

  3. 3

    Behrmann, M., Winocur, G. & Moscovitch, M. Dissociation between mental imagery and object recognition in a brain-damaged patient. Nature 359, 636–637 (1992).

  4. 4

    Kosslyn, S. M., Thompson, W. L. & Alpert, N. M. Neural systems shared by visual imagery and visual perception: a PET study. Neuroimage 6, 320–334 (1997).

  5. 5

    Roland, P. E. & Gulyas, B. Visual imagery and visual representation. Trends Neurosci. 17, 281–287 (1994).

  6. 6

    D'Esposito, M. et al. A fMRI study of mental image generation. Neuropsychologia 35, 725–730 (1997).

  7. 7

    O'Craven, K. & Kanwisher, N. Mental imagery of faces and places activates corresponding stimulus-specific brain regions. J. Cog. Neurosci. (in the press).

  8. 8

    Frith, C. & Dolan, R. J. Brain mechanisms associated with top-down processes in perception. Phil. Trans. R. Soc. Lond. 352, 1221–1230 (1997).

  9. 9

    Ishai, A. & Sagi, D. Common mechanisms of visual imagery and perception. Science 268, 1772–1774 (1995).

  10. 10

    Rainer, G., Rao, S. & Miller, E. Prospective coding for objects in primate prefrontal cortex. J. Neurosci. 19, 5493–5505 (1999).

  11. 11

    Miyashita, Y. & Chang, H. S. Neuronal correlate of pictorial short-term memory in the primate temporal cortex. Nature 331, 68–71 (1988).

  12. 12

    Tomita, H., Ohbayashi, M., Nakahara, K., Hasegawa, I. & Miyashita, Y. Top-down signal from prefrontal cortex in executive control of memory retrieval. Nature 401, 699–703 (1999).

  13. 13

    Bartolomeo, P. et al. Multiple-domain dissociation between impaired visual perception and preserved mental imagery in a patient with bilateral extrastriate lesions. Neuropsychologia 36, 239–249 (1998).

  14. 14

    Fried, I., MacDonald, K. A. & Wilson, C. Single neuron activity in human hippocampus and amygdala during recognition of faces and objects. Neuron 18, 753–765 (1997).

  15. 15

    Kreiman, G., Koch, C. & Fried, I. Category-specific visual responses of single neurons in the human medial temporal lobe. Nature Neurosci. 3, 946–953 (2000).

  16. 16

    Green, D. & Swets, J. Signal detection theory and psychophysics (Wiley, New York, 1966).

  17. 17

    Kanwisher, N. & Moscovitch, M. The cognitive neuroscience of face processing: An introduction. Cogn. Neuropsychol. 17, 1–11 (2000).

  18. 18

    Epstein, R. & Kanwisher, N. A cortical representation of the local visual environment. Nature 392, 598–601 (1998).

  19. 19

    Logothetis, N. K. & Sheinberg, D. L. Visual object recognition. Annu. Rev. Neurosci. 19, 577–621 (1996).

  20. 20

    Tanaka, K. Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 19, 109–139 (1996).

  21. 21

    Gross, C. G. How inferior temporal cortex became a visual area. Cereb. Cortex 5, 455–469 (1994).

  22. 22

    Rolls, E. Neural organization of higher visual functions. Curr. Opin. Neurobiol. 1, 274–278 (1991).

  23. 23

    Miyashita, Y. Inferior temporal cortex: Where visual perception meets memory. Annu. Rev. Neurosci. 16, 245–263 (1993).

  24. 24

    Chelazzi, L., Duncan, J., Miller, E. K. & Desimone, R. Responses of neurons in inferior temporal cortex during memory-guided visual search. J. Neurophys. 80, 2918–2940 (1998).

  25. 25

    Suzuki, W. A. Neuroanatomy of the monkey entorhinal, perirhinal and parahippocampal cortices: Organization of cortical inputs and interconnections with amygdala and striatum. Semin. Neurosci. 8, 3–12 (1996).

  26. 26

    Warrington, E. & McCarthy, R. Categories of knowledge—Further fractionations and an attempted integration. Brain 110, 1273–1296 (1987).

  27. 27

    Meunier, M., Hadfield, W., Bachevalier, J. & Murray, E. Effects of rhinal cortex lesions combined with hippocampectomy on visual recognition memory in rhesus monkeys. J. Neurophysiol. 75, 1190–1205 (1996).

  28. 28

    Fried, I., Mateer, C., Ojemann, G., Wohns, R. & Fedio, P. Organization of visuospatial functions in human cortex. Brain 105, 349–371 (1982).

  29. 29

    Ojemann, G. & Mateer, C. Human language cortex: localization of memory, syntax, and sequential motor-phoneme identification systems. Science 205, 1401–1403 (1979).

  30. 30

    Penfield, W. & Jasper, H. Epilepsy And The Functional Anatomy Of The Human Brain (Little, Brown & Co., Boston, 1954).

Download references

Acknowledgements

This work was supported by grants from NIH, the Centre for Consciousness Studies at the University of Arizona and the Keck Foundation. We thank M. Zirlinger for discussions, T. Fields, C. Wilson, E. Isham and E. Behnke for help with the recordings, F. Crick for comments and I. Wainwright for editorial assistance. We also thank all the patients who participated in these studies.

Author information

Correspondence to Itzhak Fried.

Rights and permissions

Reprints and Permissions

About this article

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.