Coherent Dynamics in the Frontal Cortex of the Behaving Monkey

Experimental Observations and Model Interpretation
  • Ad Aertsen
  • Michael Erb
  • Iris Haalman
  • Eilon Vaadia

Abstract

We have explored the hypothesis that cortical function is mediated by dynamic modulation of coherent firing in groups of neurons. Multiple single neuron activity was recorded in the frontal cortex of behaving monkeys, and analyzed for signs of correlation, using recently developed tools of dynamic correlation analysis. Correlation between neurons changed frequently within a fraction of a second, and in relation to stimuli and behavioral events. Moreover, the dynamic patterns of correlation depended on the distance between neurons. These findings support the notion that, in order to perform a computational task, neurons can associate rapidly into a functional group, while dissociating from concurrently activated competing groups. Possible mechanisms underlying such dynamic organization were investigated in spiking neural network models. We found that similar dynamic organization can be accomplished in these models, even without associated modifications of the synaptic connections. We discuss the consequences of. these findings for the spatio-temporal organization of cortical cell assemblies.

Keywords

Frontal Cortex Firing Rate Cell Assembly Spike Train Model Neuron 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abeles, M., 1982, Local Cortical Circuits. An Electrophvsiological Study. Springer: Berlin.CrossRefGoogle Scholar
  2. Abeles, M., Vaadia, E., and Bergman. H., 1990, Firing patterns of single units in the prefrontal cortex and neural network models. Network 1:13–35.Google Scholar
  3. Abeles, M., 1991, Corticonics. Neural Circuits in the Cerebral Cortex. Cambridge University Press: Cambridge, UK.CrossRefGoogle Scholar
  4. Abeles, M., Prut, Y., Bergman, H., Vaadia, E., and Aertsen. A., 1993a, Integration, synchronicity and periodicity. In: Aertsen A (ed), Brain Theory: Spatio-Temporal Aspects of Brain Function, Elsevier Science Publ.: Amsterdam, pp 149–181.Google Scholar
  5. Abeles, M., Bergman, H., Margalit, E., and Vaadia, E., 1993b, Spatio-temporal firing patterns in the frontal cortex of behaving monkeys, J Neurophysiol. 70: 1629–1643.Google Scholar
  6. Aertsen, A. M. H. J., Gerstein, G. L., Habib, M. K., and Palm, G., 1989, Dynamics of neuronal firing correlation: modulation of “effective connectivity”, J. Neurophysiol. 61: 900–917.Google Scholar
  7. Aertsen, A., and Gerstein, G., 1991, Dynamic aspects of neuronal cooperativity: Fast stimulus-locked modulations of ‘effective connectivity’. In: Krüger J (ed), Neuronal Cooperativity, Springer: Berlin, pp. 52–67.CrossRefGoogle Scholar
  8. Aertsen, A., and Preissl, H., 1991, Dynamics of activity and connectivity in physiological neuronal networks. In: Schuster H (ed), Nonlinear Dynamics and Neuronal Networks. VCH Verlag: Weinheim, pp 281–301.Google Scholar
  9. Aertsen, A., Erb, M., and Palm, G., 1994, Dynamics of functional coupling in the cerebral cortex: An attempt at a model-based interpretation, Physica D 75: 103–128.MATHCrossRefGoogle Scholar
  10. Aertsen, A., Erb, M., Palm, G., and Schüz, A., 1995a, Coherent assembly dynamics in the cortex: Multi-neuron recordings, network simulations and anatomical considerations. In: Pantev C, Elbert T, Lütkenhoner B (eds), Oscillatory Event-Related Brain Dynamics, Plenum Press: New York, pp 59–84.Google Scholar
  11. Aertsen, A., Diesmann, M., Grün, S., Arndt, M., Gewaltig, M-O., 1995b, Coupling dynamics and coincident spiking in cortical neural networks. In: Herrmann H, Pöppel E, Wolf DW (eds), Supercomputers in Brain Research: From Tomography to Neural Networks, World Scientific Publ.: Singapore, pp 213–223.Google Scholar
  12. Ahissar M, Ahissar E, Bergman H, Vaadia E., 1992a. Encoding of sound-source location and movement: Activity of single neurons and interactions between adjacent neurons in the monkey auditory cortex, J. Neurophysiol. 67: 203–215.Google Scholar
  13. Ahissar, E., Vaadia, E., Ahissar, M., Bergman, H., Arieti, A., and Abeles, M., 19926, Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context, Science 257: I412–1415.Google Scholar
  14. Barlow, H. B., 1972, Single units and sensation: A neuron doctrine for perceptual psychology? Perception 1: 371–394.CrossRefGoogle Scholar
  15. Barlow, H. B., 1992, Single cells versus neuronal assemblies. In: Aertsen, A., and Braitenberg, V. B. (cds), Information Processing in the Cortex: Experiments and Theory, Springer: Berlin, pp. 169–174.Google Scholar
  16. Bonhoeffer, T., Staiger, V. and Aertsen, A., 1989, Synaptic plasticity in rat hippocampal slice cultures: Local Hebbian’ conjunction of pre-and postsynaptic stimulation leads to distributed synaptic enhancement, Proc. Natl. Acad. Sci 86: 8113–8117.CrossRefGoogle Scholar
  17. Braitenberg, V.. 1978. Cell assemblies in the cerebral cortex. In: Heim, R., and Palm, G. (eds). Theoretical Approaches to Complex Systems. Lecture Notes in Biomathematics, Vol. 21, Springer: Berlin, pp. 171–188.CrossRefGoogle Scholar
  18. Braitenberg, V.. and Schüz, A.. 1991. Anatomy of the Cortex. Statistics and Geometry. Springer: Berlin.Google Scholar
  19. Eckhorn, R.. Bauer, R.. Jordan, W.. Brosch, M., Kruse, W., Munk, M., and Reitboeck, H. J., 1988. Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analysis in the cat. Biol. Cyhern. 60: 121–130.Google Scholar
  20. Eggermont, J. J.. 1990. The Correlative Brain. Theory and Experiment in Neural Interaction. Springer: Berlin.MATHCrossRefGoogle Scholar
  21. Eggermont, J. J.. Smith, G. M., and Bowman. D.. 1993, Spontaneous burst firing in cat primary auditory cortex: age and depth dependence and its effect on neural interaction measures, J. Neurophysiol. 69:1292–1313.Google Scholar
  22. Engel, A. K., Kreiter, A. K., König, P., and Singer, W., 1991, Interhemispheric synchronization of oscillatory responses in cat visual cortex. Science 252: 1177–1179.CrossRefGoogle Scholar
  23. Erb, M., and Aertsen. A., 1992, Dynamics of activity in biology-oriented neural network models: stability at low firing rates. In: Aertsen, A., and Braitenberg, V. (eds), Information Processing in the Cortex: Experiments and Theory, Springer: Berlin, pp. 201–223.CrossRefGoogle Scholar
  24. Fetz, E., Toyama, K., and Smith, W., 1991, Synaptic interactions between cortical neurons. In: Peters, A. (ed.), Cerebral Cortex, Vol. 9, Plenum Publ.: New York, pp. 1–47.Google Scholar
  25. Frcgnac, Y., Shulz, D., Thorpe, S., and Bienenstock, E., 1988, A cellular analogue of visual cortical plasticity, Nature 333: 367–370.CrossRefGoogle Scholar
  26. Gerstein GL, Perkel DH., 1969, Simultaneously recorded trains of action potentials: Analysis and functional interpretation. Science 164: 828–830.CrossRefGoogle Scholar
  27. Gerstein, G. L., and Perkel, D. H., 1972, Mutual temporal relationships among neuronal spike trains, Biophys. J. 12: 453–473.CrossRefGoogle Scholar
  28. Gerstein, G. L., Bloom, M. J., Espinosa, I. E., Evanczuk, S., Turner, M. R., 1983, Design of a laboratory for multi-neuron studies, IEEE Trans. Systems, Man and Cybernetics SMC-13: 668–676.Google Scholar
  29. Gerstein, G. L.. Bedenbaugh, P., AND Aertsen, A. M. H. J., 1989, Neuronal Assemblies, IEEE Trans. Biomed. Eng.36: 4–14.Google Scholar
  30. Gray, C. M., AND Singer, W., 1989, Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex, Proc. Natl. Acad. Sci. USA 86: 1698–1702.CrossRefGoogle Scholar
  31. Gray, C. M., Engel, A. K., König, P., AND Singer, W., 1992, Synchronization of oscillatory neuronal responses in cat striate cortex: temporal properties, Vs. Neurosci. 8: 337–347.CrossRefGoogle Scholar
  32. Gustafsson, B.. Wigström, H., Abraham, W. C., and Huang, Y. Y., 1987, Long term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials, J Neurosci. 7: 774–780.Google Scholar
  33. Hansel, D., and Sompolinsky, H., 1992, Synchronization and computation in chaotic neural network, Phys. Rev. Let. 68: 718–724.CrossRefGoogle Scholar
  34. Hebb, D., 1949, The Organization of Behavior. A Neuropsvchologicai Theory. Wiley: New York.Google Scholar
  35. James, W., 1890, Psychology (briefer course). In: Andersen, J. A.. and Rosenfeld. E. (eds.), Neurocomputing, MIT Press: Cambridge. (1989).Google Scholar
  36. Kaneko, K., 1990, Clustering, coding, switching, hierarchical ordering, and control in a network of chaotic elements, Physica D 41: 137–172.MathSciNetMATHCrossRefGoogle Scholar
  37. Kelso, S. R., Ganong, A. H., and Brown, T. H., 1986, Hebbian synapses in hippocampus, Proc. Natl. Acad. Sci. USA 83: 5326–5330.CrossRefGoogle Scholar
  38. Krüger, J., 1983, Simultaneous individual recordings from many cerebral neurons: techniques and results, Rei: Physiol. Biochem. Pharmacol. 98: 177–233.CrossRefGoogle Scholar
  39. Krüger, J., 1990, Multi-microelectrode investigation of monkey striate cortex: link between correlational and neuronal properties in the infragranular layers, Os. Neurosci. 5:135–142.Google Scholar
  40. Moore, G. P., Segundo, J. P., Perkel, D. H., and Levitan, H., 1970, Statistical signs of synaptic interaction in neurons, Biophys. J. 10: 876–900.CrossRefGoogle Scholar
  41. Murthy, V. N., and Fetz, E. E., 1992, Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys, Proc. Natl. Acad. Sci. USA 89: 5670–5674.CrossRefGoogle Scholar
  42. Newsome, W. T., Mikami, A., Wurtz, R. H., 1986, Motion selectivity in macaque visual cortex. III. Psycho-physics and physiology of apparent motion, J. Neurophysiol. 55:1340–1351.Google Scholar
  43. Palm, G., 1982, Neural Assemblies. An Alternative Approach to Artificial Intelligence. Springer: Berlin.Google Scholar
  44. Palm, G., Aertsen, A. M. H. J., and Gerstein, G. L., 1988, On the significance of correlations among neuronal spike trains, Biol. Cybern. 59: 1–11.MathSciNetMATHCrossRefGoogle Scholar
  45. Palm. G., 1993, On the internal structure of cell assemblies In: Aertsen, A. (ed.), Brain Theory.: Spatio-Temporal Aspects of Brain Function, Elsevier Science Publ: Amsterdam, pp. 261–270.Google Scholar
  46. Perkel, D. H., Gerstein, G. L., and Moore, G. P.. 1967, Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains, Biophys. J. 7: 419–440.CrossRefGoogle Scholar
  47. Sanes, J. N., and Donoghue, J. P., 1993, Oscillations in local field potentials of the primate motor cortex during voluntary movement, Proc. Natl. Acad. Sci. USA 90: 4470–4474.CrossRefGoogle Scholar
  48. Selemon, L. D., and Goldman Rakic, P. S., 1990, Topographic intermingling of striatonigral and striatopallidal neurons in the rhesus monkey, J. Comp. Neurol. 297: 359–376.CrossRefGoogle Scholar
  49. Toyama, K., Kimura, M., and Tanaka, K., 1981, Crosscorrelation analysis of interneuronal connectivity in cat visual cortex, J. Neurophysiol. 46: 191–201.Google Scholar
  50. Ts’o, D. Y., Gilbert, C. D., and Wiesel, T. N., 1986, Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation technique, J. Neurosci. 6: 1160–1170.Google Scholar
  51. Vaadia. E., and Aertsen, A., 1992. Coding and computation in the cortex: single-neuron activity and cooperative phenomena. In: Aertsen, A., and Braitenberg, V. (eds.), Information Processing in the Cortex: Experiments and Theory, Springer: Berlin. pp. 81–121.CrossRefGoogle Scholar
  52. Vaadia, E., Haalman, I., Abeles, M., Bergman, 1–1., Prut. Y.. Slovin, H., and Aertsen. A., 1995, Dynamics of neuronal interactions in the monkey cortex in relation to behavioral events. Nature 373: 515–518.Google Scholar
  53. von der Malsburg, C., 1981, The correlation theory of brain function, Internal Report 81–2, Max-Planck-Institute for Biophysical Chemistry, Göttingen (FRG).Google Scholar
  54. von der Malsburg, C., 1986, Am I thinking assemblies? In: Palm, G., and Aertsen, A. (eds.), Brain Theory, Springer: Berlin, pp. 161–176.Google Scholar

Copyright information

© Springer Science+Business Media New York 1996

Authors and Affiliations

  • Ad Aertsen
    • 1
  • Michael Erb
    • 2
  • Iris Haalman
    • 3
  • Eilon Vaadia
    • 3
  1. 1.Department of NeurobiologyThe Weizmann Institute of ScienceRehovotIsrael
  2. 2.Department of BiophysicsPhilipps-Universität Renthof 7MarburgGermany
  3. 3.Department of Physiology, Hadassah School of Medicine and The Center for Neural ComputationThe Hebrew UniversityJerusalemIsrael

Personalised recommendations