Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Category-specific visual responses of single neurons in the human medial temporal lobe

Nature Neuroscience volume 3, pages 946–953 (2000)Cite this article

Abstract

The hippocampus, amygdala and entorhinal cortex receive convergent input from temporal neocortical regions specialized for processing complex visual stimuli and are important in the representation and recognition of visual images. Recording from 427 single neurons in the human hippocampus, entorhinal cortex and amygdala, we found a remarkable degree of category-specific firing of individual neurons on a trial-by-trial basis. Of the recorded neurons, 14% responded selectively to visual stimuli from different categories, including faces, natural scenes and houses, famous people and animals. Based on the firing rate of individual neurons, stimulus category could be predicted with a mean probability of error of 0.24. In the hippocampus, the proportion of neurons responding to spatial layouts was greater than to other categories. Our data provide direct support for the role of human medial temporal regions in the representation of different categories of visual stimuli.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Electrode placement.
Figure 2: Sample of stimuli presented in each category.
Figure 3: Visually selective neuron in the entorhinal cortex.
Figure 4: Visually selective neuron in the hippocampus.
Figure 5: Distribution of selective neurons for each category.
Figure 6: ROC analysis and pe distribution.

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  5. 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).

    Article  CAS  Google Scholar 

  6. Leonard, C. M., Rolls, E. T., Wilson, F. A. W. & Baylis, G. C. Neurons in the amygdala of the monkey with responses selective for faces. Behav. Brain. Res 15, 159–176 (1985).

    Article  CAS  Google Scholar 

  7. Suzuki, W., Miller, E. & Desimone, R. Object and place memory in the macaque entorhinal cortex . J. Neurophysiol. 78, 1062– 1081 (1997).

    Article  CAS  Google Scholar 

  8. Miyashita, Y., Rolls, E. T., Cahusac, P. M. B., Niki, H. & Feigenbaum, J. D. Activity of hippocampal formation neurons in the monkey related to a conditional spatial response task. J. Neurophysiol. 61, 669–678 (1989).

    Article  CAS  Google Scholar 

  9. Mishkin, M. Memory in monkeys severely impaired by combined but not separate removal of amygdala and hippocampus. Nature 273, 297 –298 (1978).

    Article  CAS  Google Scholar 

  10. Meunier, M., Bachevaoer, J., Mishkin, M. & Murray, E. A. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J. Neurosci. 13, 5418–5432 (1993).

    Article  CAS  Google Scholar 

  11. Tranel, D., Damasio, H. & Damasio, A. Face agnosia and the neural substrates of memory. Annu. Rev. Neurosci. 13, 89–109 (1990).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  14. Penfield, W. & Jasper, H. Epilepsy and the Functional Anatomy of the Human Brain (Little, Brown, Boston, 1954).

    Book  Google Scholar 

  15. Treisman, A. M. & Kanwisher, N. G. Perceiving visually presented objects: recognition, awareness, and modularity. Curr. Opin. Neurobiol. 8, 218–226 (1998).

    Article  CAS  Google Scholar 

  16. Ishai, A., Ungerleider, L. G., Martin, A., Schouten, J. L. & Haxby, J. V. Distributed representation of objects in the human ventral visual pathway. Proc. Natl. Acad. Sci. USA 96, 9379–9384 (1999).

    Article  CAS  Google Scholar 

  17. Martin, A., Wiggs, C. L., Ungerleider, L. G. & Haxby, J. V. Neural correlates of category-specific knowledge. Nature 379, 649–652 (1996).

    Article  CAS  Google Scholar 

  18. Allison, T. et al. Face recognition in human extrastriate cortex. J. Neurophysiol. 71, 821–825 (1994).

    Article  CAS  Google Scholar 

  19. Nobre, A., Allison, T. & McCarthy, G. Word recognition in the human inferior temporal lobe . Nature 372, 260–263 (1994).

    Article  CAS  Google Scholar 

  20. Tong, F., Nakayama, K., Moscovitch, M., Weinrib, O. & Kanwisher, N. Response properties of the human fusiform face area. Cognit. Neuropsychol. 17, 257–279 (2000).

    Article  CAS  Google Scholar 

  21. 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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. Keeping, E. S. Introduction to Statistical Inference (Dover, New York, 1995).

    Google Scholar 

  24. Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. Impaired recognition of emotion in facial expressions following bilateral damage to the amygdala . Nature 372, 669–672 (1994).

    Article  CAS  Google Scholar 

  25. Buckley, M. J. & Gaffan, D. Perirhinal cortex ablation impairs object identification. J. Neurosci. 18, 2268–2275 (1998).

    Article  CAS  Google Scholar 

  26. 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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  28. 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 

  29. Allison, T., Puce, A., Spencer, D. & McCarthy, G. Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. Cereb. Cortex 9, 415–430 (1999).

    Article  CAS  Google Scholar 

  30. Klopp, J., Halgren, E., Marinkovic, K. & Nenov, V. Face-selective spectral changes in the human fusiform gyrus. Clin. Neurophysiol. 110, 676–682 (1999).

    Article  CAS  Google Scholar 

  31. Halgren, E., Raij, T., Marinkovic, K., Jousmaki, V. & Hari, R. Cognitive response profile of the human fusiform face area as determined by MEG. Cereb. Cortex 10, 69–81 (2000).

    Article  CAS  Google Scholar 

  32. Ojemann, J. G., Ojemann, G. A. & Lettich, E. Neuronal activity related to faces and matching in human right nondominant temporal cortex. Brain 115, 1–13 (1992).

    Article  Google Scholar 

  33. Ojemann, G. A., Ojemann, S. G. & Fried, I. Lessons from the human brain: neuronal activity related to cognition. The Neuroscientist 4, 285– 300 (1998).

    Article  Google Scholar 

  34. Scoville, W. B. & Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry. 20, 11–21 (1957).

    Article  CAS  Google Scholar 

  35. Penfield, W. & Milner, B. Memory deficit produced bilateral lesions in the hippocampal zone. Arch. Neurol. Psychol. 79, 475–479 (1958).

    Article  CAS  Google Scholar 

  36. Zola-Morgan, S. & Squire, L. R. Neuroanatomy of memory. Annu. Rev. Neurosci. 16, 547– 563 (1993).

    Article  CAS  Google Scholar 

  37. McNaughton, B. L. & Nadel, L. in Neuroscience and Connectionist Theory (ed. Seifert, W.) 1– 64 (Academic, New York, 1990).

    Google Scholar 

  38. Alvarez, P. & Squire, L. R. Memory consolidation and the medial temporal lobe: a simple network model. Proc. Natl. Acad. Sci. USA 91, 7041–7045 (1994).

    Article  CAS  Google Scholar 

  39. Treves, A. & Rolls, E. T. Computational analysis of the role of the hippocampus in memory. Hippocampus 4, 374–391 (1994).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  42. Muller, R. A quarter of a century of place cells. Cell 17, 813–822 (1996).

    CAS  Google Scholar 

  43. 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 

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

    Article  CAS  Google Scholar 

  45. Heit, G., Smith, M. E. & Halgren, E. Neural encoding of individual words and faces by the human hippocampus and amygdala. Nature 333, 773–775 (1988).

    Article  CAS  Google Scholar 

  46. Fried, I. et al. Cerebral microdialysis combined with single-neuron and electroencephalographic recording in neurosurgical patients. J. Neurosurg. 91, 697–705 (1999).

    Article  CAS  Google Scholar 

  47. Efron, B. & Tibshirani, R. J. An Introduction to the Bootstrap (Chapman & Hall/CRC, London, 1993).

    Book  Google Scholar 

  48. Yakovlev, V., Fusi, S., Berman, E. & Zohary, E. Inter-trial neuronal activity in inferior temporal cortex: a putative vehicle to generate long-term visual associations. Nat. Neurosci. 1, 310 –317 (1998).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  50. Green, D. & Swets, J. Signal Detection Theory and Psychophysics (Wiley, New York, 1966).

    Google Scholar 

Download references

Acknowledgements

This work was supported by grants from NIH (to I.F.), the Keck Foundation (to C.K.) and the Center for Consciousness Studies, University of Arizona (to I.F. and C.K.). We would like to thank D. Rozenfarb and M. Zirlinger for suggestions and reading the manuscript and Peter Steinmetz for general discussion. We wish to acknowledge Tony Fields, Jack Morrow, Eve Isham, Charles Wilson, Rick Staba, Eric Behnke and Anatol Bragin for help with the recordings.

Author information

Authors and Affiliations

  1. Computation and Neural Systems Program, California Institute of Technology, 139-74, Pasadena, 91125, California, USA

    Gabriel Kreiman & Christof Koch

  2. Division of Neurosurgery and Department of Psychiatry and Biobehavioral Sciences, Box 957039, UCLA School of Medicine, 740 Westwood Plaza, Los Angeles, 90095-7039, California, USA

    Itzhak Fried

Authors
  1. Gabriel Kreiman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christof Koch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Itzhak Fried
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Itzhak Fried.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kreiman, G., Koch, C. & Fried, I. Category-specific visual responses of single neurons in the human medial temporal lobe. Nat Neurosci 3, 946–953 (2000). https://doi.org/10.1038/78868

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/78868

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing