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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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).
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).
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).
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).
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).
Craig, J. C. Interference in identifying tactile patterns: response competition and temporal integration. Somatosens. Mot. Res. 13, 188 –213 (1996).
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).
Schneider, W. & Shiffrin, R. M. Controlled and automatic human information processing: I. Detection, search and attention. Psychol. Rev. 84, 1–66 ( 1977).
Poggio, G. F. & Viernstein, L. J. Time series analysis of impulse sequences of thalamic somatic sensory neurons. J. Neurophysiol. 27, 517–545 ( 1964).
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).
Abeles, M. Local Cortical Circuits (Springer, Berlin, Heidelberg, New York, 1982).
Eckhorn, R. et al. Coherent oscillations: a mechanism of feature linking in the visual cortex? Biol. Cybern. 60, 121– 130 (1988).
Abeles, M., Bergman, H., Margalit, E. & Vaadia, E. Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. J. Neurophysiol. 70, 1629– 1638 (1993).
Vaadia, E. et al. Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature 373, 515– 518 (1995).
Prut, Y. et al. Spatiotemporal structure of cortical activity: properties and behavioral relevance. J. Neurophysiol. 79, 2857–2874 (1998).
Haalman, I. & Vaadia, E. Emergence of spatio-temporal patterns in neuronal activity. Z. Naturforsch. 53C, 657–669 (1998).
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).
Singer, W. Synchronization of cortical activity and its putative role in information processing and learning. Annu. Rev. Physiol. 55, 349–374 (1993).
Decharms, R. C. & Merzenich, M. M. Primary cortical representation of sounds by the coordination of action potential timing. Nature 381, 610–613 ( 1996).
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).
Crick, F. & Koch, C. Towards a neurobiological theory of consciousness. Sem. Neurosci. 2, 263– 275 (1990).
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).
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).
Efron, B. & Tibshirani, R. J. An Introduction to the Bootstrap (Chapman and Hall, New York, 1993).
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).
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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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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