Correlated Activity of Neurons: A Neural Code for Higher Brain Functions?

  • Eilon Vaadia
  • Ehud Ahissar
  • Hagai Bergman
  • Yizhar Lavner
Part of the Springer Series in Synergetics book series (SSSYN, volume 49)


This chapter describes some response properties of single neurons and the interactions between them in both a sensory area (the auditory cortex) and an “association” area (the frontal cortex) of the monkey. The data described were obtained by simultaneous recording of several (6–10) neurons by six microelectrodes, in behaving animals.


Firing Rate Auditory Cortex Spike Train Effective Connectivity Neuronal Interaction 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abeles, M. (1981): The role of the cortical neuron: Integrator or coincidence detector. Isr. J. Med. Sci. 18, 83–92Google Scholar
  2. Abeles, M. (1982): Local cortical circuits: an electrophysiological study. Studies of brain function. Vol. 7 (Springer, Berlin, Heidelberg)Google Scholar
  3. Abeles, M. (1983): The quantification and graphic display of correlations among three spike trains. IEEE Trans. Biomed. Eng. BME 30, 236–239CrossRefGoogle Scholar
  4. Abeles, M. (1991) Corticonics: Neural circuits of the Cerebral Cortex. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  5. Abeles, M., Goldstein, M.H. (1977) Multiple spike train analysis. Proc. IEEE 65, 762–773CrossRefGoogle Scholar
  6. Abeles, M., Gerstein, G.L. (1988): Detecting spatiotemporal firing patterns among simultaneously recorded single neurons. J. Neurophysiol. 60, 909–923Google Scholar
  7. Abeles, M., Assaf, J., Gottlieb, Y., Hodis, H., Vaadia, E. (1975) Speculation on a neural substrate for immediate memory. Sensory Physiology and Behavior 15, 117–126Google Scholar
  8. Abeles, M., de Ribaupierre, F., de Ribaupierre, E. (1983): Detection of single unit responses which are loosely time-locked to a stimulus. IEEE Trans. Syst. Man. Cyber. SMC 13, 683–691Google Scholar
  9. Aertsen, A.M.H.J., Gerstein, G.L. (1985): Evaluation of neuronal connectivity: sensitivity of cross-correlation. Brain Res. 340, 341–354CrossRefGoogle Scholar
  10. Aertsen, A.M.H.J., Gerstein, G.L., Habib, M.K., Palm, G. (with the collaboration of P. Gochin and J. Kruger) (1989) Dynamics of neuronal firing correlation: modulation of “effective connectivity”. J. Neurophysiol. 61, 900–917Google Scholar
  11. Allum, J.H.J., Hepp-Reymond, M.C., Gysin, R. (1982): Cross-correlation analysis of interneuronal connectivity in the motor cortex of the monkey. Brain Res. 231, 325–334CrossRefGoogle Scholar
  12. Amit, D.J. (1987) The properties of models of simple neural networks. Heidelberg Colloquium on Glassy Dynamics. van Hemmen J.L. and Morgenstern I. (eds.), Springer, HeidelbergGoogle Scholar
  13. Barlow, H.B. (1972): Single units and sensation: A neuron doctrine for percepteral psychology. Perception 1, 371–394CrossRefGoogle Scholar
  14. Braitenberg, V. (1978): Cell assemblies in the cerebral cortex. Theoretical Approaches to Complex Systems. Lecture Notes in Biomathematics. Ed. by Heim R, Palm G (Springer, Berlin, Heidelberg) Vol. 21, 171–188Google Scholar
  15. Burns, D.B., Webb, A.C. (1979): The correlation between discharge times of neighboring neurons in isolated cerebral cortex. Proc. Roy. Soc. London B 203, 347–360CrossRefADSGoogle Scholar
  16. Butters, N., Pandya, D. (1969): Retention of delayed alternation: Effect of selective lesions of sulcus principalis. Science 165, 1271–1273CrossRefADSGoogle Scholar
  17. Dayhoff, J.E., Gerstein, G.L. (1983): Favoured patterns in spike trains. II. Application. J. Neurophysiol. 49, 1349–1363Google Scholar
  18. Deecke, L., Kornhuber, H.H., Lang, W., Lang, M., Schreiber, H. (1985): Timing function of the frontal cortex in sequential motor cortex in motor and learning tasks. Human Neurobiol. 4, 143–154Google Scholar
  19. Dickson, J.W., Gerstein, G.L. (1974): Interactions between neurons in auditory cortex of the cat. J. Neurophysiol. 37, 1239–1261Google Scholar
  20. Donchin, E. (ed.) (1984): Cognitive Psychophysiology. The Carmal Conferences. Vol. 1 ( Erlbaum, New Jersey )Google Scholar
  21. Eckhorn, R., Bauer, R., Jordan, W., Brosch, M., Kruse, W., Munk, M., Reitboeck, H.J. (1988): Coherent oscillations: A mechanism of feature linking in the visual cortex? Biol. Cybern. 60(2), 121–30CrossRefGoogle Scholar
  22. Edelman, G.M. (1981): Group selection as the basis for higher brain function. The organization of the cerebral cortex. Proceedings of a neuroscience research program colloquium. Ed. by Schmitt et al. ( MIT Press, Cambridge ) pp. 536–563Google Scholar
  23. Evarts, E.V., Shinoda, Y., Wise, S.P. (1984): Neurophysiological approach to higher brain function. ( Wiley, New York )Google Scholar
  24. Fetz, E.E., Gustafson, B. (1983): Relation between shapes of post-synaptic potentials and changes in firing probability of cat motoneuron. J. Physiol. (Lond.) 341, 387–410Google Scholar
  25. Frostig, R., Gottlieb, Y., Vaadia, E., Abeles, M. (1983): The effects of stimuli on the activity and functional connectivity of local neuronal groups in the cat auditory cortex. Brain Res. 272, 211–221CrossRefGoogle Scholar
  26. Fuster, J.M. (1980): The Prefrontal Cortex. Raven Press, New YorkGoogle Scholar
  27. Gassanov, U.G., Galashina, A.G., Bogdanov, A.V. (1980): A study of neuron systems activity in learning. In Neural Mechanisms of Goal-Directed Behavior and Learninged. by Thompson, R.F. et al. (Academic, New York ) pp. 341–352Google Scholar
  28. Gazanov, U.G., Galashina, A.G., Bogdanov, A.V. (1980) A study of neuron systems activity in learning. Neural Mechanisms of Goal-Directed Behavior and Learning 341–352Google Scholar
  29. Gerstein, G.L. (1988): Information flow and state in cortical neural networks: Interpreting multi-neuron experiments. In Organization of Neural Networks, Ed. by von Seelen W. et al. ( VCH, Weinheim ) pp. 53–85Google Scholar
  30. Gerstein, G.L., Aertsen, A.M.H.J. (1985): Representation of cooperative firing activity among simultaneously recorded neurons. J. Neurophysiol. 54, 1513–1526Google Scholar
  31. Gerstein, G.L., Perkel, D.H, Dayhoff, J.E. (1985): Cooperative firing activity in simultaneously recorded populations of neurons: detection and measurement. J. Neuroscience. 5, 881–889Google Scholar
  32. Goldberg, M.E., Segraves, M.A. (1987): Visuospatial and motor attention in the monkey. Neuropsychologia 25, 107–118CrossRefGoogle Scholar
  33. Goldman, P.S., Nauta, W.J.H. (1977): Columnar distribution of cortico-cortical fibers in the frontal association, limbic and motor cortex of the developing Rhesus monkey. Brain Res. 122, 393–413CrossRefGoogle Scholar
  34. Goldman-Rakic, P.S. (1987): Circuitry of primate prefrontal cortex and the regulation of behavior by representational knowledge. Mountcastle VB, Plum F (eds) The Nervous System, Vol. V, Handbook of Physiology, Am. Physiol. Soc., Bethesda, MD, pp. 373–417Google Scholar
  35. Gottlieb, Y., Vaadia, E., Abeles, M. (1989): Single unit activity in the auditory cortex of a monkey performing a short term memory to tones task. Exp. Brain Res. 74, 139–148Google Scholar
  36. Gray, C.M., Singer, W. (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl. Acad. Sci. USA, 86, 1698–1702CrossRefADSGoogle Scholar
  37. Hebb, D.O. (1949): The organization of behavior: a neuropsychological theory( Wiley, New York )Google Scholar
  38. Hopfield, J.J. (1982): Neuronal networks and physical systems with emergent collective computational abilities. Proc. Natl. Acad. Sci. USA, 79, 2554–2556CrossRefADSMathSciNetGoogle Scholar
  39. Hopfield, J.J., Tank, D.W. (1986): Computing with neural circuits: A model. Science 233, 625–633CrossRefADSGoogle Scholar
  40. Kirkwood, P.A., Sears, T.A. (1982): The effect of single afferent impulses on the probability of firing of external intercostal motoneurons in the cat. J. Physiol. 322, 315–336Google Scholar
  41. Kruger, J. (1983): Simultaneous individual recordings from many cerebral neurons: Techniques and results. Rev. Physiol. Biochem. Pharmacol. 98, 177–233CrossRefGoogle Scholar
  42. Kruger, J., Aiple, F. (1988): Multimicroelectrode investigation of monkey striate cortex: spike trains correlations in infragranular layers. J. Neurophysiol. 60, 798–828Google Scholar
  43. Levick, W.R., Cleland, B.G., Dubin, M.W. (1972): Lateral geniculate neurons of cat: Retinal inputs and physiology. Investigative Ophthalmology 1, 302–310Google Scholar
  44. Lindsey, B.G., Gerstein, G.L. (1979): Interactions among an ensemble of chordotonal organ receptors and motor neurons of the crayfish claw. J. Neurophysiol. 42, 383–399Google Scholar
  45. Lurito, J.T., Schwartz, A.B., Petrides, M., Kettner, R.E., Georgopoulos, A.P. (1988): Cross-correlations between motor cortical cells simultaneously recorded during reaching task in the monkey. Soc. Neurose. Abst. 14, 142. 5Google Scholar
  46. McNaughton, B.L., O’Keefe, J., Barnes, C.A. (1983): The stereotrode: A new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J. Neurosci. Methods 8, 391–397CrossRefGoogle Scholar
  47. Moore, G.P., Perkel, D.H., Segundo, J.P. (1966): Statistical analysis and functional interpretation of neuronal spike data. Ann. Rev. Physiol. 28, 493–522CrossRefGoogle Scholar
  48. Moore, G.P., Segundo, J.P., Perkel, D.H., Levitan, H. (1970): Statistical signs of synaptic interactions in neurons. Biophysical J. 10, 876–900CrossRefADSGoogle Scholar
  49. Murphy, J.T., Kwan, H.C., Wong, Y.C. (1985): Cross-correlation studies in primate motor cortex: Synaptic interaction and shared input. Can J Neurol. Sci. 12, 11–23Google Scholar
  50. Niki, H., Watanabe, M. (1976): Pre-frontal unit activity and delayed response: Relation to cue location versus direction of response. Brain Res. 105, 79–88CrossRefGoogle Scholar
  51. Niki, H., Watanabe, M. (1979): Prefrontal and cingulate unit activity during timing behavior in the monkey. Brain Res. 171, 213–224CrossRefGoogle Scholar
  52. Palm, G. (1982): Neural assemblies, an alternative approach to artificial intelligence. Studies of Brain Function, Vol. 7 (Springer, Berlin, Heidelberg)Google Scholar
  53. Passingham, R.E. (1975): Delayed matching after selective prefrontal lesions in monkeys (macaca mulatta). Brain Res. 92, 89–102CrossRefGoogle Scholar
  54. Perkel, D.H., Gerstein, G.L., Moore, G.P., (1967): Neuronal spike trains and stochastic point processes: II. Simultaneous spike trains. Biophys. J. 7, 419–440CrossRefGoogle Scholar
  55. Perrett, D.I., Rolls, E.T., Caan, W. (1982): Visual neurons responsive to faces in monkey temporal cortex. Exp. Brain Res. 47, 329–342CrossRefGoogle Scholar
  56. Petrides, M. (1986): The effect of periarcuate lesions in the monkey on performance of symmetrically and asymmetrically reinforced and auditory go, no-go tasks. J. Neurosci. 6, 2054–2063Google Scholar
  57. Rumelhart, D.E., Hinton, G.E., Williams, R.J. (1986): Learning internal ed. representation by error propagation. In Parallel Distributed Processing, ed. by Rumelhart DE et al. ( MIT Press, Cambridge )Google Scholar
  58. Sompolinsky, H. (1987): The theory of neural networks: the Hebb rule and beyond. Heidelberg Colloquium on Glassy Dynamics, ed. by van Hemmen JL and Morgenstern, I. (Springer, Berlin, Heidelberg. )Google Scholar
  59. Tam, D.C., Ebner, T.J., Knox, C.K. (1988): Conditional cross-interval correlation analyses with applications to simultaneously recorded cerebellar Purkinje neurons. J. Neurosci. Methods 23, 23–33CrossRefGoogle Scholar
  60. Toyama, K., Kimura, M., Tanaka, K. (1981): Crosscorrelation analysis of interneuronal connectivity in cat visual cortex. J. Neurophysiol. 46, 191–201Google Scholar
  61. Tso, D., Gilbert, C.D., Wiesel, T. (1986): Relationships between horizontal architecture in cat striate cortex as revealed by cross-correlation analysis. J. Neurosci. 6, 1160–1170Google Scholar
  62. Vaadia, E., Abeles, M. (1987): Temporal firing patterns of single units, pairs and triplets of units in the auditory cortex. J. Isr. Med. Sci. 23, 75–83Google Scholar
  63. Vaadia, E., Gottlieb, H., Abeles, M. (1982): Single unit activity related to sensorimotor association in auditory cortex of a monkey. J. Neurophysiol. 48, 201–213Google Scholar
  64. Vaadia, E., Benson, D.A., Goldstein, M.H., Hienz, R.D. (1986): Unit study of monkey frontal cortex: Active localization of auditory and visual stimuli. J. Neurophysiol. 56, 934–952Google Scholar
  65. Vaadia, E., Kurata, K., Wise, S.P. (1988): Neuronal activity preceding directional and nondirectional cues in the premotor cortex of Rhesus monkeys. Somatosensory Res. 6, 207–230CrossRefGoogle Scholar
  66. Vaadia, E., Bergman, H., Abeles, M. (1989): Neuronal activities related to higher brain functions — Theoretical and experimental implications. IEEE Trans. Biomed. Eng. 36, 25–35CrossRefGoogle Scholar
  67. Watanabe, M. (1986): Prefrontal unit activity during delayed conditional Go/NoGo discrimination in Monkey I. Relation to stimulus. Brain Res. 382, 1–14CrossRefGoogle Scholar
  68. Wise, S.P., Mauritz, K.H. (1985): Set related neuronal activity in the premotor cortex of rhesus monkeys: effects of changes in motor set. Proc. R. Soc. Lond. B 223, 331–354CrossRefADSGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1991

Authors and Affiliations

  • Eilon Vaadia
    • 1
  • Ehud Ahissar
    • 1
  • Hagai Bergman
    • 1
  • Yizhar Lavner
    • 1
  1. 1.Department of Physiology, Hadassah Medical SchoolThe Hebrew UniversityJerusalemIsrael

Personalised recommendations