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Attention modulates synchronized neuronal firing in primate somatosensory cortex

Abstract

A potentially powerful information processing strategy in the brain is to take advantage of the temporal structure of neuronal spike trains. An increase in synchrony within the neural representation of an object or location increases the efficacy of that neural representation at the next synaptic stage in the brain; thus, increasing synchrony is a candidate for the neural correlate of attentional selection1. We investigated the synchronous firing of pairs of neurons in the secondary somatosensory cortex (SII) of three monkeys trained to switch attention between a visual task and a tactile discrimination task. We found that most neuron pairs in SII cortex fired synchronously and, furthermore, that the degree of synchrony was affected by the monkey's attentional state. In the monkey performing the most difficult task, 35% of neuron pairs that fired synchronously changed their degree of synchrony when the monkey switched attention between the tactile and visual tasks. Synchrony increased in 80% and decreased in 20% of neuron pairs affected by attention.

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Figure 1: Responses of a typical neuron pair in monkey M2.
Figure 2: Shift predictor corrected cross-correlograms (SCCCs).

References

  1. 1

    Niebur, E. & Koch, C. A model for the neuronal implementation of selective visual attention based on temporal correlation among neurons. J. Comput. Neurosci. 1, 141– 158 (1994).

    CAS  Article  Google Scholar 

  2. 2

    Hsiao, S. S., O'Shaughnessy, D M. & Johnson, K. O. Effects of selective attention on spatial form processing in monkey primary and secondary somatosensory cortex. J. Neurophysiol. 70, 444–447 ( 1993).

    CAS  Article  Google Scholar 

  3. 3

    Mountcastle, V. B., Reitboeck, H. J., Poggio, G. F. & Steinmetz, M. A. Adaptation of the Reitboeck method of multiple microelectrode recording to the neocortex of the waking monkey. J. Neurosci. Methods 36, 77–84 (1991).

    CAS  Article  Google Scholar 

  4. 4

    Poranen, A. & Hyvärinen, J. Effects of attention on multiunit responses to vibrations in the somatosensory regions of the monkey's brain. EEG Clin. Neurophysiol. 53, 525– 537 (1982).

    CAS  Article  Google Scholar 

  5. 5

    Burton, H., Sinclair, R. J., Hon, S.-Y. & Whang, K. C. Tactile-spatial and cross-modal attention effects in the second somatosensory and 7b cortical areas of rhesus monkey. Somatosens. Mot. Res. 14, 237–267 (1997).

    CAS  Article  Google Scholar 

  6. 6

    Craig, J. C. Interference in identifying tactile patterns: response competition and temporal integration. Somatosens. Mot. Res. 13, 188 –213 (1996).

    Article  Google Scholar 

  7. 7

    Shiffrin, R. M. & Schneider, W. Controlled and automatic human information processing: II. Perceptual learning, automatic attending and a general theory. Psychol. Rev. 84, 127–190 (1977).

    Article  Google Scholar 

  8. 8

    Schneider, W. & Shiffrin, R. M. Controlled and automatic human information processing: I. Detection, search and attention. Psychol. Rev. 84, 1–66 ( 1977).

    Article  Google Scholar 

  9. 9

    Poggio, G. F. & Viernstein, L. J. Time series analysis of impulse sequences of thalamic somatic sensory neurons. J. Neurophysiol. 27, 517–545 ( 1964).

    CAS  Article  Google Scholar 

  10. 10

    Perkel, D. H., Gerstein, G. L. & Moore, G. P. Neuronal spike trains and stochastic point processes. II: Simultaneous spike trains. Biophys. J. 7, 419–440 (1967).

    CAS  Article  Google Scholar 

  11. 11

    Abeles, M. Local Cortical Circuits (Springer, Berlin, Heidelberg, New York, 1982).

    Book  Google Scholar 

  12. 12

    Eckhorn, R. et al. Coherent oscillations: a mechanism of feature linking in the visual cortex? Biol. Cybern. 60, 121– 130 (1988).

    CAS  Article  Google Scholar 

  13. 13

    Abeles, M., Bergman, H., Margalit, E. & Vaadia, E. Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. J. Neurophysiol. 70, 1629– 1638 (1993).

    CAS  Article  Google Scholar 

  14. 14

    Vaadia, E. et al. Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature 373, 515– 518 (1995).

    ADS  CAS  Article  Google Scholar 

  15. 15

    Prut, Y. et al. Spatiotemporal structure of cortical activity: properties and behavioral relevance. J. Neurophysiol. 79, 2857–2874 (1998).

    CAS  Article  Google Scholar 

  16. 16

    Haalman, I. & Vaadia, E. Emergence of spatio-temporal patterns in neuronal activity. Z. Naturforsch. 53C, 657–669 (1998).

    Article  Google Scholar 

  17. 17

    Murthy, V. N. & Fetz, E. E. Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. J. Neurophysiol. 76, 3968– 3982 (1996).

    CAS  Article  Google Scholar 

  18. 18

    Singer, W. Synchronization of cortical activity and its putative role in information processing and learning. Annu. Rev. Physiol. 55, 349–374 (1993).

    CAS  Article  Google Scholar 

  19. 19

    Decharms, R. C. & Merzenich, M. M. Primary cortical representation of sounds by the coordination of action potential timing. Nature 381, 610–613 ( 1996).

    ADS  CAS  Article  Google Scholar 

  20. 20

    Roy, S. & Calloway, K. D. Synchronization of Local Neural Networks in the Somatosensory Cortex. A Comparison of Stationary and Moving Stimuli. J. Neurophysiol. 81, 999– 1013 (1999).

    CAS  Article  Google Scholar 

  21. 21

    Crick, F. & Koch, C. Towards a neurobiological theory of consciousness. Sem. Neurosci. 2, 263– 275 (1990).

    Google Scholar 

  22. 22

    DiCarlo, J. J., Lane, J. W., Hsiao, S. S. & Johnson, K. O. Marking microelectrode penetrations with fluorescent dyes. J. Neurosci. Methods 54, 75–81 ( 1996).

    Article  Google Scholar 

  23. 23

    Brody, C. D. Slow covariations in neuronal resting potentials can lead to artefactually fast cross-correlations in their spike trains. J. Neurophysiol. 80, 3345–3351 ( 1998).

    CAS  Article  Google Scholar 

  24. 24

    Efron, B. & Tibshirani, R. J. An Introduction to the Bootstrap (Chapman and Hall, New York, 1993).

    Book  Google Scholar 

  25. 25

    Roy, A., Steinmetz, P. N., Johnson, K. O. & Niebur, E. Model-free detection of synchrony in neuronal spike trains, with an application to primate somatosensory cortex. Neurocomputing (in the press).

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Acknowledgements

This work was supported by the NIH, the NSF and the Alfred P. Sloan Foundation. We thank J. DiCarlo, M. Usher and S. Yantis for discussions and J. Lane for technical support.

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Correspondence to E. Niebur.

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Steinmetz, P., Roy, A., Fitzgerald, P. et al. Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature 404, 187–190 (2000). https://doi.org/10.1038/35004588

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