Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 1999 May 7;266(1422):875–881. doi: 10.1098/rspb.1999.0718

Neuronal population activity and functional imaging.

J W Scannell 1, M P Young 1
PMCID: PMC1689920  PMID: 10380677

Abstract

Human functional brain imaging detects blood flow changes that are thought to reflect the activity of neuronal populations and, thus, the responses of neurons that carry behaviourally relevant information. Since this relationship is poorly understood, we explored the link between the activity of single neurons and their neuronal population. The functional imaging results were in good agreement with levels of population activation predicted from the known effects of sensory stimulation, learning and attention on single cortical neurons. However, the nature of the relationship between population activation and single neuron firing was very surprising. Population activation was strongly influenced by those neurons firing at low rates and so was very sensitive to the baseline or 'spontaneous' firing rate. When neural representations were sparse and neurons were tuned to several stimulus dimensions, population activation was hardly influenced by the few neurons whose firing was most strongly modulated by the task or stimulus. Measures of population activation could miss changes in information processing given simultaneous changes in neurons' baseline firing, response modulation or tuning width. Factors that can modulate baseline firing, such as attention, may have a particularly large influence on population activation. The results have implications for the interpretation of functional imaging signals and for cross-calibration between different methods for measuring neuronal activity.

Full Text

The Full Text of this article is available as a PDF (356.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albright T. D. Direction and orientation selectivity of neurons in visual area MT of the macaque. J Neurophysiol. 1984 Dec;52(6):1106–1130. doi: 10.1152/jn.1984.52.6.1106. [DOI] [PubMed] [Google Scholar]
  2. Arieli A., Shoham D., Hildesheim R., Grinvald A. Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual cortex. J Neurophysiol. 1995 May;73(5):2072–2093. doi: 10.1152/jn.1995.73.5.2072. [DOI] [PubMed] [Google Scholar]
  3. Arieli A., Sterkin A., Grinvald A., Aertsen A. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science. 1996 Sep 27;273(5283):1868–1871. doi: 10.1126/science.273.5283.1868. [DOI] [PubMed] [Google Scholar]
  4. Baddeley R., Abbott L. F., Booth M. C., Sengpiel F., Freeman T., Wakeman E. A., Rolls E. T. Responses of neurons in primary and inferior temporal visual cortices to natural scenes. Proc Biol Sci. 1997 Dec 22;264(1389):1775–1783. doi: 10.1098/rspb.1997.0246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boynton G. M., Engel S. A., Glover G. H., Heeger D. J. Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci. 1996 Jul 1;16(13):4207–4221. doi: 10.1523/JNEUROSCI.16-13-04207.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Britten K. H., Shadlen M. N., Newsome W. T., Movshon J. A. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci. 1992 Dec;12(12):4745–4765. doi: 10.1523/JNEUROSCI.12-12-04745.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Connor C. E., Preddie D. C., Gallant J. L., Van Essen D. C. Spatial attention effects in macaque area V4. J Neurosci. 1997 May 1;17(9):3201–3214. doi: 10.1523/JNEUROSCI.17-09-03201.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Corbetta M., Miezin F. M., Dobmeyer S., Shulman G. L., Petersen S. E. Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography. J Neurosci. 1991 Aug;11(8):2383–2402. doi: 10.1523/JNEUROSCI.11-08-02383.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Crick F., Jones E. Backwardness of human neuroanatomy. Nature. 1993 Jan 14;361(6408):109–110. doi: 10.1038/361109a0. [DOI] [PubMed] [Google Scholar]
  10. Douglas R. J., Koch C., Mahowald M., Martin K. A., Suarez H. H. Recurrent excitation in neocortical circuits. Science. 1995 Aug 18;269(5226):981–985. doi: 10.1126/science.7638624. [DOI] [PubMed] [Google Scholar]
  11. Engel S. A., Glover G. H., Wandell B. A. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex. 1997 Mar;7(2):181–192. doi: 10.1093/cercor/7.2.181. [DOI] [PubMed] [Google Scholar]
  12. Fahy F. L., Riches I. P., Brown M. W. Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex. Exp Brain Res. 1993;96(3):457–472. doi: 10.1007/BF00234113. [DOI] [PubMed] [Google Scholar]
  13. Friston K. J., Price C. J., Fletcher P., Moore C., Frackowiak R. S., Dolan R. J. The trouble with cognitive subtraction. Neuroimage. 1996 Oct;4(2):97–104. doi: 10.1006/nimg.1996.0033. [DOI] [PubMed] [Google Scholar]
  14. Földiák P. Forming sparse representations by local anti-Hebbian learning. Biol Cybern. 1990;64(2):165–170. doi: 10.1007/BF02331346. [DOI] [PubMed] [Google Scholar]
  15. Gallant J. L., Connor C. E., Van Essen D. C. Neural activity in areas V1, V2 and V4 during free viewing of natural scenes compared to controlled viewing. Neuroreport. 1998 Jan 5;9(1):85–90. doi: 10.1097/00001756-199801050-00017. [DOI] [PubMed] [Google Scholar]
  16. Georgopoulos A. P., Schwartz A. B., Kettner R. E. Neuronal population coding of movement direction. Science. 1986 Sep 26;233(4771):1416–1419. doi: 10.1126/science.3749885. [DOI] [PubMed] [Google Scholar]
  17. Grinvald A., Lieke E. E., Frostig R. D., Hildesheim R. Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J Neurosci. 1994 May;14(5 Pt 1):2545–2568. doi: 10.1523/JNEUROSCI.14-05-02545.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jueptner M., Stephan K. M., Frith C. D., Brooks D. J., Frackowiak R. S., Passingham R. E. Anatomy of motor learning. I. Frontal cortex and attention to action. J Neurophysiol. 1997 Mar;77(3):1313–1324. doi: 10.1152/jn.1997.77.3.1313. [DOI] [PubMed] [Google Scholar]
  19. Kadekaro M., Vance W. H., Terrell M. L., Gary H., Jr, Eisenberg H. M., Sokoloff L. Effects of antidromic stimulation of the ventral root on glucose utilization in the ventral horn of the spinal cord in the rat. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5492–5495. doi: 10.1073/pnas.84.15.5492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Knight B. W. The relationship between the firing rate of a single neuron and the level of activity in a population of neurons. Experimental evidence for resonant enhancement in the population response. J Gen Physiol. 1972 Jun;59(6):767–778. doi: 10.1085/jgp.59.6.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kristan W. B., Jr, Shaw B. K. Population coding and behavioral choice. Curr Opin Neurobiol. 1997 Dec;7(6):826–831. doi: 10.1016/s0959-4388(97)80142-0. [DOI] [PubMed] [Google Scholar]
  22. Luck S. J., Chelazzi L., Hillyard S. A., Desimone R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J Neurophysiol. 1997 Jan;77(1):24–42. doi: 10.1152/jn.1997.77.1.24. [DOI] [PubMed] [Google Scholar]
  23. Malonek D., Grinvald A. Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science. 1996 Apr 26;272(5261):551–554. doi: 10.1126/science.272.5261.551. [DOI] [PubMed] [Google Scholar]
  24. Miyashita Y. Neuronal correlate of visual associative long-term memory in the primate temporal cortex. Nature. 1988 Oct 27;335(6193):817–820. doi: 10.1038/335817a0. [DOI] [PubMed] [Google Scholar]
  25. Motter B. C. Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. J Neurophysiol. 1993 Sep;70(3):909–919. doi: 10.1152/jn.1993.70.3.909. [DOI] [PubMed] [Google Scholar]
  26. Motter B. C. Neural correlates of attentive selection for color or luminance in extrastriate area V4. J Neurosci. 1994 Apr;14(4):2178–2189. doi: 10.1523/JNEUROSCI.14-04-02178.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Newsome W. T., Britten K. H., Movshon J. A. Neuronal correlates of a perceptual decision. Nature. 1989 Sep 7;341(6237):52–54. doi: 10.1038/341052a0. [DOI] [PubMed] [Google Scholar]
  28. Peters A., Payne B. R., Budd J. A numerical analysis of the geniculocortical input to striate cortex in the monkey. Cereb Cortex. 1994 May-Jun;4(3):215–229. doi: 10.1093/cercor/4.3.215. [DOI] [PubMed] [Google Scholar]
  29. Petersen S. E., Fox P. T., Posner M. I., Mintun M., Raichle M. E. Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature. 1988 Feb 18;331(6157):585–589. doi: 10.1038/331585a0. [DOI] [PubMed] [Google Scholar]
  30. Poeppel D. A critical review of PET studies of phonological processing. Brain Lang. 1996 Dec;55(3):317–385. doi: 10.1006/brln.1996.0108. [DOI] [PubMed] [Google Scholar]
  31. Raichle M. E. Behind the scenes of functional brain imaging: a historical and physiological perspective. Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):765–772. doi: 10.1073/pnas.95.3.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Raichle M. E., Fiez J. A., Videen T. O., MacLeod A. M., Pardo J. V., Fox P. T., Petersen S. E. Practice-related changes in human brain functional anatomy during nonmotor learning. Cereb Cortex. 1994 Jan-Feb;4(1):8–26. doi: 10.1093/cercor/4.1.8. [DOI] [PubMed] [Google Scholar]
  33. Rolls E. T., Treves A., Tovee M. J., Panzeri S. Information in the neuronal representation of individual stimuli in the primate temporal visual cortex. J Comput Neurosci. 1997 Nov;4(4):309–333. doi: 10.1023/a:1008899916425. [DOI] [PubMed] [Google Scholar]
  34. Sakai K., Miyashita Y. Neural organization for the long-term memory of paired associates. Nature. 1991 Nov 14;354(6349):152–155. doi: 10.1038/354152a0. [DOI] [PubMed] [Google Scholar]
  35. Shadlen M. N., Newsome W. T. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci. 1998 May 15;18(10):3870–3896. doi: 10.1523/JNEUROSCI.18-10-03870.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sobotka S., Ringo J. L. Investigation of long-term recognition and association memory in unit responses from inferotemporal cortex. Exp Brain Res. 1993;96(1):28–38. doi: 10.1007/BF00230436. [DOI] [PubMed] [Google Scholar]
  37. Somers D. C., Nelson S. B., Sur M. An emergent model of orientation selectivity in cat visual cortical simple cells. J Neurosci. 1995 Aug;15(8):5448–5465. doi: 10.1523/JNEUROSCI.15-08-05448.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tagamets M. A., Horwitz B. Integrating electrophysiological and anatomical experimental data to create a large-scale model that simulates a delayed match-to-sample human brain imaging study. Cereb Cortex. 1998 Jun;8(4):310–320. doi: 10.1093/cercor/8.4.310. [DOI] [PubMed] [Google Scholar]
  39. Tootell R. B., Reppas J. B., Kwong K. K., Malach R., Born R. T., Brady T. J., Rosen B. R., Belliveau J. W. Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J Neurosci. 1995 Apr;15(4):3215–3230. doi: 10.1523/JNEUROSCI.15-04-03215.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Treue S., Maunsell J. H. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature. 1996 Aug 8;382(6591):539–541. doi: 10.1038/382539a0. [DOI] [PubMed] [Google Scholar]
  41. Yarowsky P., Kadekaro M., Sokoloff L. Frequency-dependent activation of glucose utilization in the superior cervical ganglion by electrical stimulation of cervical sympathetic trunk. Proc Natl Acad Sci U S A. 1983 Jul;80(13):4179–4183. doi: 10.1073/pnas.80.13.4179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zeki S. M. Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J Physiol. 1974 Feb;236(3):549–573. doi: 10.1113/jphysiol.1974.sp010452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. van Vreeswijk C., Sompolinsky H. Chaotic balanced state in a model of cortical circuits. Neural Comput. 1998 Aug 15;10(6):1321–1371. doi: 10.1162/089976698300017214. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES