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Invariant visual representation by single neurons in the human brain

Abstract

It takes a fraction of a second to recognize a person or an object even when seen under strikingly different conditions. How such a robust, high-level representation is achieved by neurons in the human brain is still unclear1,2,3,4,5,6. In monkeys, neurons in the upper stages of the ventral visual pathway respond to complex images such as faces and objects and show some degree of invariance to metric properties such as the stimulus size, position and viewing angle2,4,7,8,9,10,11,12. We have previously shown that neurons in the human medial temporal lobe (MTL) fire selectively to images of faces, animals, objects or scenes13,14. Here we report on a remarkable subset of MTL neurons that are selectively activated by strikingly different pictures of given individuals, landmarks or objects and in some cases even by letter strings with their names. These results suggest an invariant, sparse and explicit code, which might be important in the transformation of complex visual percepts into long-term and more abstract memories.

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References

  1. 1

    Barlow, H. Single units and sensation: a neuron doctrine for perception. Perception 1, 371–394 (1972)

  2. 2

    Gross, C. G., Bender, D. B. & Rocha-Miranda, C. E. Visual receptive fields of neurons in inferotemporal cortex of the monkey. Science 166, 1303–1306 (1969)

  3. 3

    Konorski, J. Integrative Activity of the Brain (Univ. Chicago Press, Chicago, 1967)

  4. 4

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

  5. 5

    Riesenhuber, M. & Poggio, T. Neural mechanisms of object recognition. Curr. Opin. Neurobiol. 12, 162–168 (2002)

  6. 6

    Young, M. P. & Yamane, S. Sparse population coding of faces in the inferior temporal cortex. Science 256, 1327–1331 (1992)

  7. 7

    Logothetis, N. K., Pauls, J. & Poggio, T. Shape representation in the inferior temporal cortex of monkeys. Curr. Biol. 5, 552–563 (1995)

  8. 8

    Logothetis, N. K. & Pauls, J. Psychophysical and physiological evidence for viewer-centered object representations in the primate. Cereb. Cortex 3, 270–288 (1995)

  9. 9

    Perrett, D., Rolls, E. & Caan, W. Visual neurons responsive to faces in the monkey temporal cortex. Exp. Brain Res. 47, 329–342 (1982)

  10. 10

    Schwartz, E. L., Desimone, R., Albright, T. D. & Gross, C. G. Shape recognition and inferior temporal neurons. Proc. Natl Acad. Sci. USA 80, 5776–5778 (1983)

  11. 11

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

  12. 12

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

  13. 13

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

  14. 14

    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)

  15. 15

    Macmillan, N. A. & Creelman, C. D. Detection Theory: A User's Guide (Cambridge Univ. Press, New York, 1991)

  16. 16

    Picton, T. The P300 wave of the human event-related potential. J. Clin. Neurophysiol. 9, 456–479 (1992)

  17. 17

    Halgren, E., Marinkovic, K. & Chauvel, P. Generators of the late cognitive potentials in auditory and visual oddball tasks. Electroencephalogr. Clin. Neurophysiol. 106, 156–164 (1998)

  18. 18

    McCarthy, G., Wood, C. C., Williamson, P. D. & Spencer, D. D. Task-dependent field potentials in human hippocampal formation. J. Neurosci. 9, 4253–4268 (1989)

  19. 19

    Saleem, K. S. & Tanaka, K. Divergent projections from the anterior inferotemporal area TE to the perirhinal and entorhinal cortices in the macaque monkey. J. Neurosci. 16, 4757–4775 (1996)

  20. 20

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

  21. 21

    Kanwisher, N., McDermott, J. & Chun, M. M. The fusiform face area: A module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302–4311 (1997)

  22. 22

    Haxby, J. V. et al. Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293, 2425–2430 (2001)

  23. 23

    Eichenbaum, H. A cortical-hippocampal system for declarative memory. Nature Rev. Neurosci. 1, 41–50 (2000)

  24. 24

    Hampson, R. E., Pons, P. P., Stanford, T. R. & Deadwyler, S. A. Categorization in the monkey hippocampus: A possible mechanism for encoding information into memory. Proc. Natl Acad. Sci. USA 101, 3184–3189 (2004)

  25. 25

    Squire, L. R., Stark, C. E. L. & Clark, R. E. The medial temporal lobe. Annu. Rev. Neurosci. 27, 279–306 (2004)

  26. 26

    Mishashita, Y. Neuronal correlate of visual associative long-term memory in the primate temporal cortex. Nature 335, 817–820 (1988)

  27. 27

    Koch, C. The Quest for Consciousness: A Neurobiological Approach (Roberts, Englewood, Colorado, 2004)

  28. 28

    Wilson, M. A. & McNaughton, B. L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055–1058 (1993)

  29. 29

    Ekstrom, A. D. et al. Cellular networks underlying human spatial navigation. Nature 425, 184–187 (2003)

  30. 30

    Quian Quiroga, R., Nadasdy, Z. & Ben-Shaul, Y. Unsupervised spike detection and sorting with wavelets and super-paramagnetic clustering. Neural Comput. 16, 1661–1687 (2004)

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Acknowledgements

We thank all patients for their participation; P. Sinha for drawing some faces; colleagues for providing pictures; I. Wainwright for administrative assistance; and E. Behnke, T. Fields, E. Ho, E. Isham, A. Kraskov, P. Steinmetz, I. Viskontas and C. Wilson for technical assistance. This work was supported by grants from the NINDS, NIMH, NSF, DARPA, the Office of Naval Research, the W.M. Keck Foundation Fund for Discovery in Basic Medical Research, a Whiteman fellowship (to G.K.), the Gordon Moore Foundation, the Sloan Foundation, and the Swartz Foundation for Computational Neuroscience.

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Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Correspondence to R. Quian Quiroga.

Supplementary information

  1. Supplementary Notes

    This contains Supplementary Methods and Legends to accompany Supplementary Figures S1-11. (PDF 4435 kb)

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Further reading

Figure 1: A single unit in the left posterior hippocampus activated exclusively by different views of the actress Jennifer Aniston.
Figure 2: A single unit in the right anterior hippocampus that responds to pictures of the actress Halle Berry (conventions as in Fig. 1).
Figure 3: A multi-unit in the left anterior hippocampus that responds to photographs of the Sydney Opera House and the Baha'i Temple (conventions as in Fig. 1).
Figure 4: Distribution of the area under the ROC curves for the 51 units (out of 132 responsive units) showing an invariant representation.

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