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Object-based attention involves the sequential activation of feature-specific cortical modules

Nature Neuroscience volume 17, pages 619–624 (2014)Cite this article

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Abstract

Object-based theories of attention propose that the selection of an object's feature leads to the rapid selection of all other constituent features, even those that are task irrelevant. We used magnetoencephalographic recordings to examine the timing and sequencing of neural activity patterns in feature-specific cortical areas as human subjects performed an object-based attention task. Subjects attended to one of two superimposed moving dot arrays that were perceived as transparent surfaces on the basis either of color or speed of motion. When surface motion was attended, the magnetoencephalographic waveforms showed enhanced activity in the motion-specific cortical area starting at ∼150 ms after motion onset, followed after ∼60 ms by enhanced activity in the color-specific area. When surface color was attended, this temporal sequence was reversed. This rapid sequential activation of the relevant and irrelevant feature modules provides a neural basis for the binding of an object's features into a unitary perceptual experience.

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Figure 1: Stimuli for experiments 1 and 2.
Figure 2: The sensory effects of color and motion.
Figure 3: Effect of attention on motion processing in color-absent conditions.
Figure 4: Experiment 1: sequential selection of attended motion feature and unattended color feature.
Figure 5: Experiment 2: sequential selection of attended color feature and unattended motion feature.
Figure 6: Source waveforms showing timing of sensory effects and relevant and irrelevant feature selections.

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Acknowledgements

We would like to thank M. Wachter for help with the data collection and N. Nönnig and M. Scholz for technical support. This work was supported by grants Scho1217/1-2 and SFB779 TP A1 from the Deutsche Forschungsgemeinschaft (DFG) and by grants from the US National Science Foundation (BCS-1029084) and the National Institute of Mental Health (1P50MH86385).

Author information

Authors and Affiliations

  1. Department of Neurology, Otto-von-Guericke University, Magdeburg, Germany

    Mircea A Schoenfeld, Jens-Max Hopf, Christian Merkel & Hans-Jochen Heinze

  2. Department of Behavioral Neurology, Leibniz Institute for Neurobiology, Magdeburg, Germany

    Mircea A Schoenfeld, Jens-Max Hopf, Christian Merkel, Hans-Jochen Heinze & Steven A Hillyard

  3. Kliniken Schmieder, Allensbach, Germany

    Mircea A Schoenfeld

  4. Department of Neurosciences, University of California at San Diego, LaJolla, California, USA

    Steven A Hillyard

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  1. Mircea A Schoenfeld
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Contributions

M.A.S. designed and performed the experiments, analyzed the data and wrote the paper. J.-M.H. designed the experiments and analyzed the data. C.M. analyzed the data. H.-J.H. supervised the performance of the experiments and data analysis. S.A.H. designed the experiments, supervised the performance of the experiments and data analysis, and wrote the paper.

Corresponding author

Correspondence to Mircea A Schoenfeld.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Source activity waveforms from experiment 1

The two traces at the top show the averaged source activity waveforms for motion sensitive sources in the middle occipital gyri (red tracing) and color sensitive sources in inferior occipital cortex (blue tracing) from Experiment 1, where selection of the surface was based on motion speed and color was the task-irrelevant feature. The subsequent four source activity waveforms (red tracings) originate from left and right motion-sensitive sources in the middle occipital gyri obtained from the analysis of the differences formed by subtracting the ERF on grey-slow*/red-fast trials from the ERF on grey-slow/red-fast* trials (first two red waveforms) and grey-fast/red-slow* trials from ERFs on grey-fast*/ red-slow trials (last two red waveforms). The bottom four source activity waveforms (blue tracings) originate from left and right color-sensitive sources in the inferior occipital cortex obtained from the differences formed by subtracting the ERF on grey-slow*/red-fast trials from the ERF on grey-slow/red-fast* trials (first two blue waveforms) and grey-fast/red-slow* trials from ERFs on grey-fast*/ red-slow trials (last two blue waveforms). Note that all waveform deflections are positive (upwards) regardless of the sign of the subtractions, since these waveforms depict positive current density measures.

Supplementary Figure 2 Source activity waveforms from experiment 2

The two traces at the top show the averaged source activity waveforms for color sensitive sources in inferior occipital cortex (blue tracing) and motion sensitive sources in the middle occipital gyri (red tracing) from Experiment 2, where selection of the surface was based on color and motion was the task-irrelevant feature. The subsequent four source activity waveforms (blue tracings) originate from left and right color-sensitive sources in the inferior occipital cortex obtained from the differences formed by subtracting the grey-slow*/red-fast trials from ERFs on grey-slow/red-fast* trials (first two blue waveforms) and subtracting the grey-fast*/red-slow trials from ERFs on grey-fast/red-slow* (last two blue waveforms). The bottom four source activity waveforms (red tracings) originate from left and right motion-sensitive sources in the middle occipital gyri obtained from the differences formed by subtracting the grey-slow*/red-fast trials from ERFs on grey-slow/red-fast* trials (first two red waveforms) and subtracting the grey-fast*/red-slow trials from ERFs on grey-fast/red-slow* (last two red waveforms).

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Schoenfeld, M., Hopf, JM., Merkel, C. et al. Object-based attention involves the sequential activation of feature-specific cortical modules. Nat Neurosci 17, 619–624 (2014). https://doi.org/10.1038/nn.3656

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