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Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory

Abstract

Selective attention filters information to limit what is encoded and maintained in working memory. Although the prefrontal cortex (PFC) is central to both selective attention and working memory, the underlying neural processes that link these cognitive abilities remain elusive. Using functional magnetic resonance imaging to guide repetitive transcranial magnetic stimulation with electroencephalographic recordings in humans, we perturbed PFC function at the inferior frontal junction in participants before they performed a selective-attention, delayed-recognition task. This resulted in diminished top-down modulation of activity in posterior cortex during early encoding stages, which predicted a subsequent decrement in working memory accuracy. Participants with stronger fronto-posterior functional connectivity displayed greater disruptive effects. Our data further suggests that broad alpha-band (7–14 Hz) phase coherence subserved this long-distance top-down modulation. These results suggest that top-down modulation mediated by the prefrontal cortex is a causal link between early attentional processes and subsequent memory performance.

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Figure 1: Experimental procedure.
Figure 2: Functional connectivity analysis revealed a fronto-parietal region associated with both motion and color top-down modulation, the right IFJ.
Figure 3: Behavioral results.
Figure 4: Attentional modulation of the P1 during color processing and motion processing.
Figure 5: Neuro-behavioral correlations.
Figure 6: Alpha-band phase coherence between right-frontal and central-posterior regions immediately preceding the onset of color stimuli.

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References

  1. Posner, M.I. Orienting of attention. Q. J. Exp. Psychol. 32, 3–25 (1980).

    Article  CAS  Google Scholar 

  2. Baddeley, A. Working Memory (Oxford University Press, Oxford, 1986).

  3. Duncan, J. & Humphreys, G.W. Visual search and stimulus similarity. Psychol. Rev. 96, 433–458 (1989).

    Article  CAS  Google Scholar 

  4. Näätänen, R. Processing negativity: an evoked potential reflection of selective attention. Psychol. Bull. 92, 605–640 (1982).

    Article  Google Scholar 

  5. LaBar, K.S., Gitelman, D.R., Parrish, T.B. & Mesulam, M. Neuroanatomic overlap of working memory and spatial attention networks: a functional MRI comparison within subjects. Neuroimage 10, 695–704 (1999).

    Article  CAS  Google Scholar 

  6. Awh, E. & Jonides, J. Overlapping mechanisms of attention and spatial working memory. Trends Cogn. Sci. 5, 119–126 (2001).

    Article  CAS  Google Scholar 

  7. Kastner, S. & Ungerleider, L.G. Mechanisms of visual attention in the human cortex. Annu. Rev. Neurosci. 23, 315–341 (2000).

    Article  CAS  Google Scholar 

  8. Gazzaley, A., Cooney, J.W., McEvoy, K., Knight, R.T. & D'Esposito, M. Top-down enhancement and suppression of the magnitude and speed of neural activity. J. Cogn. Neurosci. 17, 507–517 (2005).

    Article  Google Scholar 

  9. Rainer, G., Asaad, W.F. & Miller, E.K. Selective representation of relevant information by neurons in the primate prefrontal cortex. Nature 393, 577–579 (1998).

    Article  CAS  Google Scholar 

  10. Moran, J. & Desimone, R. Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784 (1985).

    Article  CAS  Google Scholar 

  11. Fuster, J.M., Bauer, R.H. & Jervey, J.P. Functional interactions between inferotemporal and prefrontal cortex in a cognitive task. Brain Res. 330, 299–307 (1985).

    Article  CAS  Google Scholar 

  12. Zanto, T.P. & Gazzaley, A. Neural suppression of irrelevant information underlies optimal working memory performance. J. Neurosci. 29, 3059–3066 (2009).

    Article  CAS  Google Scholar 

  13. Rutman, A.M., Clapp, W.C., Chadick, J.Z. & Gazzaley, A. Early top-down control of visual processing predicts working memory performance. J. Cogn. Neurosci. 22, 1224–1234 (2010).

    Article  Google Scholar 

  14. Ungerleider, L.G., Gaffan, D. & Pelak, V.S. Projections from inferior temporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkeys. Exp. Brain Res. 76, 473–484 (1989).

    Article  CAS  Google Scholar 

  15. Webster, M.J., Bachevalier, J. & Ungerleider, L.G. Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb. Cortex 4, 470–483 (1994).

    Article  CAS  Google Scholar 

  16. Rossi, A.F., Pessoa, L., Desimone, R. & Ungerleider, L.G. The prefrontal cortex and the executive control of attention. Exp. Brain Res. 192, 489–497 (2009).

    Article  Google Scholar 

  17. Corbetta, M. & Shulman, G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 (2002).

    Article  CAS  Google Scholar 

  18. Gazzaley, A. et al. Functional interactions between prefrontal and visual association cortex contribute to top-down modulation of visual processing. Cereb. Cortex 17, i125–i135 (2007).

    Article  Google Scholar 

  19. Barceló, F., Suwazono, S. & Knight, R.T. Prefrontal modulation of visual processing in humans. Nat. Neurosci. 3, 399–403 (2000).

    Article  Google Scholar 

  20. Taylor, P.C.J., Nobre, A.C. & Rushworth, M.F.S. FEF TMS affects visual cortical activity. Cereb. Cortex 17, 391–399 (2007).

    Article  Google Scholar 

  21. Capotosto, P., Babiloni, C., Romani, G.L. & Corbetta, M. Frontoparietal cortex controls spatial attention through modulation of anticipatory alpha rhythms. J. Neurosci. 29, 5863–5872 (2009).

    Article  CAS  Google Scholar 

  22. Ruff, C.C. et al. Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. Cereb. Cortex 18, 817–827 (2008).

    Article  Google Scholar 

  23. Miller, B.T., Vytlacil, J., Fegen, D., Pradhan, S. & D'Esposito, M. The prefrontal cortex modulates category selectivity in human extrastriate cortex. J. Cogn. Neurosci. 23, 1–10 (2011).

    Article  Google Scholar 

  24. Zanto, T.P., Rubens, M.T., Bollinger, J. & Gazzaley, A. Top-down modulation of visual feature processing: the role of the inferior frontal junction. Neuroimage 53, 736–745 (2010).

    Article  Google Scholar 

  25. Zanto, T.P., Toy, B. & Gazzaley, A. Delays in neural processing during working memory encoding in normal aging. Neuropsychologia 48, 13–25 (2010).

    Article  Google Scholar 

  26. Zhang, W. & Luck, S.J. Feature-based attention modulates feedforward visual processing. Nat. Neurosci. 12, 24–25 (2009).

    Article  Google Scholar 

  27. Klimesch, W., Freunberger, R. & Sauseng, P. Oscillatory mechanisms of process binding in memory. Neurosci. Biobehav. Rev. 34, 1002–1014 (2010).

    Article  Google Scholar 

  28. Zeki, S. et al. A direct demonstration of functional specialization in human visual cortex. J. Neurosci. 11, 641–649 (1991).

    Article  CAS  Google Scholar 

  29. Chawla, D., Rees, G. & Friston, K.J. The physiological basis of attentional modulation in extrastriate visual areas. Nat. Neurosci. 2, 671–676 (1999).

    Article  CAS  Google Scholar 

  30. Rissman, J., Gazzaley, A. & D'Esposito, M. Measuring functional connectivity during distinct stages of a cognitive task. Neuroimage 23, 752–763 (2004).

    Article  Google Scholar 

  31. Gazzaley, A., Rissman, J. & Desposito, M. Functional connectivity during working memory maintenance. Cogn. Affect. Behav. Neurosci. 4, 580–599 (2004).

    Article  Google Scholar 

  32. Pascual-Leone, A. et al. Study and modulation of human cortical excitability with transcranial magnetic stimulation. J. Clin. Neurophysiol. 15, 333–343 (1998).

    Article  CAS  Google Scholar 

  33. Thut, G. & Pascual-Leone, A. A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience. Brain Topogr. 22, 219–232 (2010).

    Article  Google Scholar 

  34. Anllo-Vento, L. & Hillyard, S.A. Selective attention to the color and direction of moving stimuli: electrophysiological correlates of hierarchical feature selection. Percept. Psychophys. 58, 191–206 (1996).

    Article  CAS  Google Scholar 

  35. Morishima, Y. et al. Task-specific signal transmission from prefrontal cortex in visual selective attention. Nat. Neurosci. 12, 85–91 (2009).

    Article  CAS  Google Scholar 

  36. Fuggetta, G., Pavone, E.F., Walsh, V., Kiss, M. & Eimer, M. Cortico-cortical interactions in spatial attention: a combined ERP/TMS study. J. Neurophysiol. 95, 3277–3280 (2006).

    Article  Google Scholar 

  37. Gazzaley, A. et al. Age-related top-down suppression deficit in the early stages of cortical visual memory processing. Proc. Natl. Acad. Sci. USA 105, 13122–13126 (2008).

    Article  CAS  Google Scholar 

  38. Silver, M.A. & Kastner, S. Topographic maps in human frontal and parietal cortex. Trends Cogn. Sci. 13, 488–495 (2009).

    Article  Google Scholar 

  39. Derrfuss, J., Brass, M. & von Cramon, D.Y. Cognitive control in the posterior frontolateral cortex: evidence from common activations in task coordination, interference control and working memory. Neuroimage 23, 604–612 (2004).

    Article  Google Scholar 

  40. Brass, M. & von Cramon, D.Y. Decomposing components of task preparation with functional magnetic resonance imaging. J. Cogn. Neurosci. 16, 609–620 (2004).

    Article  Google Scholar 

  41. Ungerleider, L.G., Courtney, S.M. & Haxby, J.V. A neural system for human visual working memory. Proc. Natl. Acad. Sci. USA 95, 883–890 (1998).

    Article  CAS  Google Scholar 

  42. Sauseng, P. & Klimesch, W. What does phase information of oscillatory brain activity tell us about cognitive processes? Neurosci. Biobehav. Rev. 32, 1001–1013 (2008).

    Article  Google Scholar 

  43. Thut, G., Nietzel, A., Brandt, S.A. & Pascual-Leone, A. Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. J. Neurosci. 26, 9494–9502 (2006).

    Article  CAS  Google Scholar 

  44. Sauseng, P., Klimesch, W., Schabus, M. & Doppelmayr, M. Fronto-parietal EEG coherence in theta and upper alpha reflect central executive functions of working memory. Int. J. Psychophysiol. 57, 97–103 (2005).

    Article  Google Scholar 

  45. Bollinger, J., Rubens, M.T., Zanto, T.P. & Gazzaley, A. Expectation-driven changes in cortical functional connectivity influence working-memory and long-term memory performance. J. Neurosci. 30, 14399–14410 (2010).

    Article  CAS  Google Scholar 

  46. Desimone, R., Miller, E.K. & Chelazzi, L. Interaction of neural systems for attention and memory. in Large-Scale Theories of Neuronal Function (eds. C. Koch & J. Davis) 75–91 (MIT Press, Cambridge, Massachusetts, 1994).

  47. Awh, E., Vogel, E.K. & Oh, S.H. Interactions between attention and working memory. Neuroscience 139, 201–208 (2006).

    Article  CAS  Google Scholar 

  48. Schoenfeld, M.A. et al. Spatio-temporal analysis of feature-based attention. Cereb. Cortex 17, 2468–2477 (2007).

    Article  CAS  Google Scholar 

  49. Grave de Peralta Menendez, R., Murray, M.M., Michel, C.M., Martuzzi, R. & Andino, S.L.G. Electrical neuroimaging based on biophysical constraints. Neuroimage 21, 527–539 (2004).

    Article  Google Scholar 

  50. Lachaux, J.P., Rodriguez, E., Martinerie, J. & Varela, F.J. Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8, 194–208 (1999).

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank V. Barres and C. Gruson-Daniel for their assistance. This work was supported by US National Institutes of Health grants 1F32AG030249-01A2 (T.P.Z.) and 5R01AG030395 (A.G.).

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Authors

Contributions

T.P.Z., A.T. and A.G. conceptualized and designed the task. T.P.Z. and M.T.R. performed the experiment. T.P.Z. analyzed the data. T.P.Z. and A.G. wrote the paper.

Corresponding authors

Correspondence to Theodore P Zanto or Adam Gazzaley.

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The authors declare no competing financial interests.

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Supplementary Figures 1–3, Supplementary Tables 1 and 2, Supplementary Results and Supplementary Discussion (PDF 801 kb)

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Zanto, T., Rubens, M., Thangavel, A. et al. Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory. Nat Neurosci 14, 656–661 (2011). https://doi.org/10.1038/nn.2773

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