In crowded visual scenes, attention is needed to select relevant stimuli. To study the underlying mechanisms, we recorded neurons in cortical area V4 while macaque monkeys attended to behaviorally relevant stimuli and ignored distracters. Neurons activated by the attended stimulus showed increased gamma-frequency (35 to 90 hertz) synchronization but reduced low-frequency (<17 hertz) synchronization compared with neurons at nearby V4 sites activated by distracters. Because postsynaptic integration times are short, these localized changes in synchronization may serve to amplify behaviorally relevant signals in the cortex.
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Desimone R., Duncan J., Annu. Rev. Neurosci. 18, 193 (1995).
J. Moran, R. Desimone Science 229, 782 (1985).
Chelazzi L., Miller E. K., Duncan J., Desimone R., Nature 363, 345 (1993).
Treue S., Maunsell J. H., Nature 382, 539 (1996).
Luck S. J., Chelazzi L., Hillyard S. A., Desimone R., J. Neurophysiol. 77, 24 (1997).
Reynolds J. H., Chelazzi L., Desimone R., J. Neurosci. 19, 1736 (1999).
Motter B. C., J. Neurophysiol. 70, 909 (1993).
Gray C. M., König P., Engel A. K., Singer W., Nature 338, 334 (1989).
Crick F., Koch C., Semin. Neurosci. 2, 263 (1990).
Niebur E., Koch C., Rosin C., Vision Res. 33, 2789 (1993).
Murthy V. N., Fetz E. E., J. Neurophysiol. 76, 3968 (1996).
Makeig S., Jung T. P., Brain Res. Cogn. Brain Res. 4, 15 (1996).
Roelfsema P. R., Engel A. K., König P., Singer W., Nature 385, 157 (1997).
Fries P., Roelfsema P. R., Engel A. K., König P., Singer W., Proc. Natl. Acad. Sci. U.S.A. 94, 12699 (1997).
Donoghue J. P., Sanes J. N., Hatsopoulos N. G., Gaal G., J. Neurophysiol. 79, 159 (1998).
Gruber T., Müller M. M., Keil A., Elbert T., Clin. Neurophysiol. 110, 2074 (1999).
Maldonado P. E., Friedman-Hill S., Gray C. M., Cereb. Cortex 10, 1117 (2000).
Salinas E., Sejnowski T. J., J. Neurosci. 20, 6193 (2000).
Steinmetz P. N., et al., Nature 404, 187 (2000).
Animal care was in accordance with NIH guidelines. Standard procedures were used to record spike and LFP activity simultaneously from four extracellular electrodes in V4 of two monkeys (electrode separations of 650 or 900 μm; Plexon data acquisition system). The LFP (filtered at 1 to 100 Hz) reflects the average transmembrane currents of neurons in a volume of a few hundred micrometers radius around the electrode tip (41). Negative values of LFP correspond to neuronal activation. Spike waveforms were stored for offline sorting. We pooled all neurons recorded through a given electrode [≈2 to 10 neurons; see supplementary information (24)]. The resulting multi-unit almost always showed clear oscillatory synchronization. Analysis of single units revealed that some showed much stronger oscillatory synchronization than others. Whenever there was clear oscillatory synchronization, attention effects were essentially identical, irrespective of whether the spikes were pooled or from an isolated neuron.
The cue directing attention was either a short (0.75°) line next to the fixation spot, pointing to the location of the target, or the fixation spot color, with red cueing the upper stimulus and green, the lower stimulus. The delay between cue and stimulus onset was 1500 to 2000 ms, and the cue remained throughout the trial. In a subset of recordings, we used a blocked trial design without any explicit cue. All paradigms gave essentially the same results. Stimuli were pure luminance gratings (100% contrast, 2° to 3° diameter, 1° to 2°/s drift rate, one to two cycles per degree of spatial frequency) with a frame rate of 120 Hz. The grating inside the RF had the optimal orientation to coactivate cells at as many of the electrodes as possible. The grating outside the RF was always in another quadrant and orthogonal to the inside RF grating, and did not activate the recorded neurons. After a random interval of 500 to 5000 ms, the white stripes of the cued (target) stimulus changed to isoluminant yellow. The color change was close to the monkey's detection threshold, ensuring that the task could be performed only when attention was focused on the target. The monkey was rewarded if it maintained fixation throughout the trial and released a bar within 650 ms of the color change. In half of the trials, the same color change occurred for the uncued (distracter) stimulus. Responses to distracter changes resulted in a time-out without reward. Performance was 83 to 87% correct. We recorded 100 to 300 correct trials per attention condition. Eye position for the two attention conditions differed by 16 arcmin (delay) to 13 arcmin (stimulus period).
We calculated STAs by averaging all LFP segments at ±150 ms around all spikes recorded under one attentional condition. Only STAs of LFPs and spikes recorded from separate electrodes were used in the analyses. However, STAs of LFPs and spikes recorded on a single electrode showed essentially identical effects. For the analysis of the sustained response, the 300 ms after stimulus onset was discarded because it always contained stimulus-locked modulations in the LFP. Thereafter, stimulus-locked components were largely absent and shift-predictor STAs flat. For direct comparisons between sustained response synchronization and firing rates, only spikes used for STA compilation were used. We also calculated cycle-triggered averages (CTAs) of spike times (11) by band-pass filtering the LFP in a predefined range and triggering the spike-time averaging by troughs in the filtered LFP. After normalization for average spike rate, CTAs give changes in firing rate around cycle triggers. The CTAs showed qualitatively the same attention effects as STAs. Cross-correlation histograms (CCHs) of spike times proved much less sensitive than STAs in detecting oscillatory synchronization. STAs often revealed oscillatory synchronization where CCHs did not. See supplementary information (24) for a comparison of the different measures.
M. S. Worden, J. J. Foxe, N. Wang, G.V. Simpson, J. Neurosci. (Online) 20, RC63 (2000).
Supplementary data are available on Science Online at
For statistical analysis, we used the frequency bands that were obvious from the SFC spectra. Results remain essentially unchanged for small variations (±6.7 Hz). Unless stated otherwise, we used a paired Sign test.
Reynolds J. H., Pasternak T., Desimone R., Neuron 26, 703 (2000).
S. Treue, D. R. Patzwahl, paper presented at the 30th Annual Meeting of the Society for Neuroscience, New Orleans, LA, 6 November 2000.
Cross-correlations between monitor refreshes and either spikes or LFP showed no sign of locking. Thus, early gamma-frequency synchronization was locked to stimulus onset but not to stimulus flicker.
We compared firing rates (1-ms bin width) for the two attentional conditions across all recording sites using a paired t test. The first five consecutive significant (P < 0.05) bins defined the onset of consistent attentional modulation.
Munk M. H., Roelfsema P. R., König P., Engel A. K., Singer W., Science 272, 271 (1996).
E. H. Buhl, G. Tamas, A. Fisahn, J. Physiol. 513 117 (1998).
Alonso J. M., Usrey W. M., Reid R. C., Nature 383, 815 (1996).
R, Azouz,
Gray C. M., Proc. Natl. Acad. Sci. U.S.A. 97, 8110 (2000).
Ahmed B., Anderson J. C., Douglas R. J., Martin K. A., Whitteridge D., Cereb. Cortex 8, 462 (1998).
Spitzer H., Desimone R., Moran J., Science 240, 338 (1988).
Connor C. E., Gallant J. L., Preddie D. C., Van Essen D. C., J. Neurophysiol. 75, 1306 (1996).
McAdams C. J., Maunsell J. H. R., J. Neurosci. 19, 431 (1999).
Andersen R. A., Essick G. K., Siegel R. M., Science 230, 456 (1985).
Olshausen B. A., Anderson C. H., Van Essen D. C., J. Neurosci. 13, 4700 (1993).
Salinas E., Abbott L. F., Proc. Natl. Acad. Sci. U.S.A. 93, 11956 (1996).
Frost J. D., Electroencephalogr. Clin. Neurophysiol. 23, 89 (1967).
We thank Plexon Incorporated for technical assistance, A. Rossi for help during the experiments, and F. Crick, C. Gray, and C. Koch for valuable comments on the manuscript.

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Published In

Volume 291 | Issue 5508
23 February 2001

Submission history

Received: 5 September 2000
Accepted: 22 December 2000
Published in print: 23 February 2001


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Pascal Fries*
Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Building 49, Room 1B80, 9000 Rockville Pike, Bethesda, MD 20892–4415, USA.
John H. Reynolds
Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Building 49, Room 1B80, 9000 Rockville Pike, Bethesda, MD 20892–4415, USA.
Systems Neurobiology Laboratory, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037–1099, USA.
Alan E. Rorie
Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Building 49, Room 1B80, 9000 Rockville Pike, Bethesda, MD 20892–4415, USA.
Robert Desimone
Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Building 49, Room 1B80, 9000 Rockville Pike, Bethesda, MD 20892–4415, USA.


To whom correspondence should be addressed. E-mail: [email protected]

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