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Distinct neural mechanisms of distractor suppression in the frontal and parietal lobe

Abstract

The posterior parietal cortex and the prefrontal cortex are associated with eye movements and visual attention, but their specific contributions are poorly understood. We compared the dorsolateral prefrontal cortex (dlPFC) and the lateral intraparietal area (LIP) in monkeys using a memory saccade task in which a salient distractor flashed at a variable timing and location during the memory delay. We found that the two areas had similar responses to target selection, but made distinct contributions to distractor suppression. Distractor responses were more strongly suppressed and more closely correlated with performance in the dlPFC relative to LIP. Moreover, reversible inactivation of the dlPFC produced much larger increases in distractibility than inactivation of LIP. These findings suggest that LIP and dlPFC mediate different aspects of selective attention. Although both areas can contribute to the perceptual selection of salient information, the dlPFC has a decisive influence on whether and how attended stimulus is linked with actions.

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Figure 1: Task and behavioral performance.
Figure 2: Neural responses in LIP and dlPFC.
Figure 3: Correspondence between distractor responses and error rates.
Figure 4: Analysis of error trials.
Figure 5: Anticipatory and visual suppression.
Figure 6: Effects of reversible inactivation of LIP and dlPFC.

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References

  1. Badre, D. & Wagner, A.D. Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia 45, 2883–2901 (2007).

    Article  Google Scholar 

  2. 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 

  3. Egeth, H.E. & Yantis, S. Visual attention: control, representation, and time course. Annu. Rev. Psychol. 48, 269–297 (1997).

    Article  CAS  Google Scholar 

  4. Bays, P.M., Singh-Curry, V., Gorgoraptis, N., Driver, J. & Husain, M. Integration of goal- and stimulus-related visual signals revealed by damage to human parietal cortex. J. Neurosci. 30, 5968–5978 (2010).

    Article  CAS  Google Scholar 

  5. Klingberg, T. Development of a superior frontal-intraparietal network for visuo-spatial working memory. Neuropsychologia 44, 2171–2177 (2006).

    Article  Google Scholar 

  6. Doyle, A.E. Executive functions in attention-deficit/hyperactivity disorder. J. Clin. Psychiatry 67, 21–26 (2006).

    PubMed  Google Scholar 

  7. Brown, G.G. & Thompson, W.K. Functional brain imaging in schizophrenia: selected results and methods. Curr. Top. Behav. Neurosci. 4, 181–214 (2010).

    Article  Google Scholar 

  8. Gottlieb, J. From thought to action: the parietal cortex as a bridge between perception, action, and cognition. Neuron 53, 9–16 (2007).

    Article  CAS  Google Scholar 

  9. Chafee, M.V. & Goldman-Rakic, P.S. Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. J. Neurophysiol. 83, 1550–1566 (2000).

    Article  CAS  Google Scholar 

  10. Chafee, M.V. & Goldman-Rakic, P.S. Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. J. Neurophysiol. 79, 2919–2940 (1998).

    Article  CAS  Google Scholar 

  11. Goldman-Rakic, P.S. Cellular basis of working memory. Neuron 14, 477–485 (1995).

    Article  CAS  Google Scholar 

  12. Miller, E.K. & Cohen, J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).

    Article  CAS  Google Scholar 

  13. Wardak, C., Olivier, E. & Duhamel, J.R. A deficit in covert attention after parietal cortex inactivation in the monkey. Neuron 42, 501–508 (2004).

    Article  CAS  Google Scholar 

  14. Wardak, C., Olivier, E. & Duhamel, J.R. Saccadic target selection deficits after lateral intraparietal area inactivation in monkeys. J. Neurosci. 22, 9877–9884 (2002).

    Article  CAS  Google Scholar 

  15. Balan, P.F. & Gottlieb, J. Functional significance of nonspatial information in monkey lateral intraparietal area. J. Neurosci. 29, 8166–8176 (2009).

    Article  CAS  Google Scholar 

  16. Sawaguchi, T. & Iba, M. Prefrontal cortical representation of visuospatial working memory in monkeys examined by local inactivation with muscimol. J. Neurophysiol. 86, 2041–2053 (2001).

    Article  CAS  Google Scholar 

  17. Wardak, C., Ibos, G., Duhamel, J.R. & Olivier, E. Contribution of the monkey frontal eye field to covert visual attention. J. Neurosci. 26, 4228–4235 (2006).

    Article  CAS  Google Scholar 

  18. Moore, T. & Armstrong, K.M. Selective gating of visual signals by microstimulation of frontal cortex. Nature 421, 370–373 (2003).

    Article  CAS  Google Scholar 

  19. Premereur, E., Vanduffel, W., Roelfsema, P.R. & Janssen, P. Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area. J. Neurophysiol. 108, 1392–1402 (2012).

    Article  Google Scholar 

  20. Premereur, E., Vanduffel, W. & Janssen, P. Functional heterogeneity of macaque lateral intraparietal neurons. J. Neurosci. 31, 12307–12317 (2011).

    Article  CAS  Google Scholar 

  21. Buschman, T.J. & Miller, E.K. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315, 1860–1862 (2007).

    Article  CAS  Google Scholar 

  22. Katsuki, F. & Constantinidis, C. Early involvement of prefrontal cortex in visual bottom-up attention. Nat. Neurosci. 15, 1160–1166 (2012).

    Article  CAS  Google Scholar 

  23. Bisley, J.W. & Goldberg, M.E. Neural correlates of attention and distractibility in the lateral intraparietal area. J. Neurophysiol. 95, 1696–1717 (2006).

    Article  Google Scholar 

  24. Bisley, J.W. & Goldberg, M.E. Neuronal activity in the lateral intraparietal area and spatial attention. Science 299, 81–86 (2003).

    Article  CAS  Google Scholar 

  25. Powell, K.D. & Goldberg, M.E. Response of neurons in the lateral intraparietal area to a distractor flashed during the delay period of a memory-guided saccade. J. Neurophysiol. 84, 301–310 (2000).

    Article  CAS  Google Scholar 

  26. Bisley, J.W. & Goldberg, M. Attention, intention, and priority in the parietal lobe. Annu. Rev. Neurosci. 33, 1–21 (2010).

    Article  CAS  Google Scholar 

  27. Katsuki, F. & Constantinidis, C. Unique and shared roles of the posterior parietal and dorsolateral prefrontal cortex in cognitive functions. Front. Integr. Neurosci. 6, 17 (2012).

    Article  Google Scholar 

  28. Mayo, J.P. & Sommer, M.A. Neuronal adaptation caused by sequential visual stimulation in the frontal eye field. J. Neurophysiol. 100, 1923–1935 (2008).

    Article  Google Scholar 

  29. Purcell, B.A., Schall, J.D., Logan, G.D. & Palmeri, T.J. From salience to saccades: multiple-alternative gated stochastic accumulator model of visual search. J. Neurosci. 32, 3433–3446 (2012).

    Article  CAS  Google Scholar 

  30. Schall, J.D., Purcell, B.A., Heitz, R.P., Logan, G.D. & Palmeri, T.J. Neural mechanisms of saccade target selection: gated accumulator model of the visual-motor cascade. Eur. J. Neurosci. 33, 1991–2002 (2011).

    Article  Google Scholar 

  31. Lo, C.C. & Wang, X.J. Cortico-basal ganglia circuit mechanism for a decision threshold in reaction time tasks. Nat. Neurosci. 9, 956–963 (2006).

    Article  CAS  Google Scholar 

  32. Isoda, M. & Hikosaka, O. Switching from automatic to controlled action by monkey medial frontal cortex. Nat. Neurosci. 10, 240–248 (2007).

    Article  CAS  Google Scholar 

  33. Hasegawa, R.P., Peterson, B.W. & Goldberg, M.E. Prefrontal neurons coding suppression of specific saccades. Neuron 43, 415–425 (2004).

    Article  CAS  Google Scholar 

  34. Kowler, E., Anderson, E., Dosher, B. & Blaser, E. The role of attention in the programming of saccades. Vision Res. 35, 1897–1916 (1995).

    Article  CAS  Google Scholar 

  35. Theeuwes, J. Top-down and bottom-up control of visual selection. Acta Psychol. (Amst.) 135, 77–99 (2010).

    Article  Google Scholar 

  36. Noudoost, B. & Moore, T. Control of visual cortical signals by prefrontal dopamine. Nature 474, 372–375 (2011).

    Article  CAS  Google Scholar 

  37. Anderson, J.C., Kennedy, H. & Martin, K.A. Pathways of attention: synaptic relationships of frontal eye field to V4, lateral intraparietal cortex, and area 46 in macaque monkey. J. Neurosci. 31, 10872–10881 (2011).

    Article  CAS  Google Scholar 

  38. Reynolds, J.H. & Heeger, D.J. The normalization model of attention. Neuron 61, 168–185 (2009).

    Article  CAS  Google Scholar 

  39. Pearce, J.M. & Mackintosh, N.J. Two Theories of Attention: a Review and a Possible Integration (Oxford University Press, New York, 2010).

  40. Wang, X.J. Attractor network models. in Encyclopedia of Neuroscience (ed. L.R. Squire) 667–679 (Academic Press, Oxford, 2009).

  41. Furman, M. & Wang, X.J. Similarity effect and optimal control of multiple-choice decision making. Neuron 60, 1153–1168 (2008).

    Article  CAS  Google Scholar 

  42. Brunel, N. & Wang, X.J. Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition. J. Comput. Neurosci. 11, 63–85 (2001).

    Article  CAS  Google Scholar 

  43. Compte, A., Brunel, N., Goldman-Rakic, P.S. & Wang, X.J. Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb. Cortex 10, 910–923 (2000).

    Article  CAS  Google Scholar 

  44. Ganguli, S. et al. One-dimensional dynamics of attention and decision making in LIP. Neuron 58, 15–25 (2008).

    Article  CAS  Google Scholar 

  45. Wang, X.J., Tegner, J., Constantinidis, C. & Goldman-Rakic, P.S. Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory. Proc. Natl. Acad. Sci. USA 101, 1368–1373 (2004).

    Article  CAS  Google Scholar 

  46. Kisvárday, Z.F. et al. One axon-multiple functions: specificity of lateral inhibitory connections by large basket cells. J. Neurocytol. 31, 255–264 (2002).

    Article  Google Scholar 

  47. Boehnke, S.E. et al. Visual adaptation and novelty responses in the superior colliculus. Eur. J. Neurosci. 34, 766–779 (2011).

    Article  Google Scholar 

  48. Somogyi, P., Tamas, G., Lujan, R. & Buhl, E.H. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res. Rev. 26, 113–135 (1998).

    Article  CAS  Google Scholar 

  49. Silberberg, G. & Markram, H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53, 735–746 (2007).

    Article  CAS  Google Scholar 

  50. Oristaglio, J., Schneider, D.M., Balan, P.F. & Gottlieb, J. Integration of visuospatial and effector information during symbolically cued limb movements in monkey lateral intraparietal area. J. Neurosci. 26, 8310–8319 (2006).

    Article  CAS  Google Scholar 

  51. Bruce, C.J., Goldberg, M.E., Stanton, G.B. & Bushnell, M.C. Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. J. Neurophysiol. 54, 714–734 (1985).

    Article  CAS  Google Scholar 

  52. Barash, S., Bracewell, R.M., Fogassi, L., Gnadt, J.W. & Andersen, R.A. Saccade-related activity in the lateral intraparietal area. I. Temporal properties; comparison with area 7a. J. Neurophysiol. 66, 1095–1108 (1991).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank M. Golberg, D. Salzman and V. Ferrera for their comments on an earlier version of the manuscript. This work was supported by a Swiss National Science Foundation Fellowship (PBELB-120948) and a Human Frontier Science Program Cross-Disciplinary Fellowship to M.S. (LT00934/2008-C).

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M.S. and J.G. conceived the experiment. M.S. collected and analyzed the data. J.G. wrote the manuscript.

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Correspondence to Jacqueline Gottlieb.

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The authors declare no competing financial interests.

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Suzuki, M., Gottlieb, J. Distinct neural mechanisms of distractor suppression in the frontal and parietal lobe. Nat Neurosci 16, 98–104 (2013). https://doi.org/10.1038/nn.3282

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