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Prefrontal neurons transmit signals to parietal neurons that reflect executive control of cognition

Nature Neuroscience volume 16, pages 1484–1491 (2013)Cite this article

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Abstract

Prefrontal cortex influences behavior largely through its connections with other association cortices; however, the nature of the information conveyed by prefrontal output signals and what effect these signals have on computations performed by target structures is largely unknown. To address these questions, we simultaneously recorded the activity of neurons in prefrontal and posterior parietal cortices of monkeys performing a rule-based spatial categorization task. Parietal cortex receives direct prefrontal input, and parietal neurons, like their prefrontal counterparts, exhibit signals that reflect rule-based cognitive processing in this task. By analyzing rapid fluctuations in the cognitive information encoded by activity in the two areas, we obtained evidence that signals reflecting rule-dependent categories were selectively transmitted in a top-down direction from prefrontal to parietal neurons, suggesting that prefrontal output is important for the executive control of distributed cognitive processing.

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Figure 1: Dynamic spatial categorization task, behavioral performance and network representation of spatial categories.
Figure 2: The transmission analysis applied to hypothetical ensembles containing two category-selective neurons in prefrontal and parietal cortex.
Figure 3: Lag 1 transmission of category signals between prefrontal and parietal neurons.
Figure 4: Dependence of lag 1 transmission on the simultaneity of neuronal activity recorded in parietal and prefrontal cortex.
Figure 5: Sign of top-down and bottom-up interactions at lag 1.
Figure 6: Significance and sign of transmission as a function of the lag between the posterior probability time series associated with vertical category representation in prefrontal and parietal cortex.
Figure 7: Network transmission of vertical category signals is modulated by behavioral performance.

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References

  1. Medalla, M. & Barbas, H. Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure. Eur. J. Neurosci. 23, 161–179 (2006).

    Article  CAS  PubMed  Google Scholar 

  2. Schwartz, M.L. & Goldman-Rakic, P.S. Callosal and intrahemispheric connectivity of the prefrontal association cortex in rhesus monkey: relation between intraparietal and principal sulcal cortex. J. Comp. Neurol. 226, 403–420 (1984).

    Article  CAS  PubMed  Google Scholar 

  3. Cavada, C. & Goldman-Rakic, P.S. Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J. Comp. Neurol. 287, 422–445 (1989).

    Article  CAS  PubMed  Google Scholar 

  4. Andersen, R.A., Asanuma, C., Essick, G. & Siegel, R.M. Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule. J. Comp. Neurol. 296, 65–113 (1990).

    Article  CAS  PubMed  Google Scholar 

  5. Goldman-Rakic, P.S. Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. in. Handbook of Physiology: The Nervous System: Higher Functions of the Brain (eds. Mountcastle, V.B., Plum, F. & Geiger, S.R.) 373–417 (Am. Physiol. Soc., Bethesda, Maryland, USA, 1987).

  6. Andersen, R.A. & Cui, H. Intention, action planning, and decision making in parietal-frontal circuits. Neuron 63, 568–583 (2009).

    Article  CAS  PubMed  Google Scholar 

  7. Qi, X.L. et al. Comparison of neural activity related to working memory in primate dorsolateral prefrontal and posterior parietal cortex. Front Syst. Neurosci 4, 12 (2010).

    PubMed  PubMed Central  Google Scholar 

  8. 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  PubMed  Google Scholar 

  9. Funahashi, S., Chafee, M.V. & Goldman-Rakic, P.S. Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task. Nature 365, 753–756 (1993).

    Article  CAS  PubMed  Google Scholar 

  10. Gnadt, J.W. & Andersen, R.A. Memory related motor planning activity in posterior parietal cortex of macaque. Exp. Brain Res. 70, 216–220 (1988).

    CAS  PubMed  Google Scholar 

  11. 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  PubMed  Google Scholar 

  12. Nieder, A. & Miller, E.K. A parieto-frontal network for visual numerical information in the monkey. Proc. Natl. Acad. Sci. USA 101, 7457–7462 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Nieder, A., Freedman, D.J. & Miller, E.K. Representation of the quantity of visual items in the primate prefrontal cortex. Science 297, 1708–1711 (2002).

    Article  CAS  PubMed  Google Scholar 

  14. Vallentin, D. & Nieder, A. Representations of visual proportions in the primate posterior parietal and prefrontal cortices. Eur. J. Neurosci. 32, 1380–1387 (2010).

    Article  PubMed  Google Scholar 

  15. Tudusciuc, O. & Nieder, A. Contributions of primate prefrontal and posterior parietal cortices to length and numerosity representation. J. Neurophysiol. 101, 2984–2994 (2009).

    Article  PubMed  Google Scholar 

  16. Swaminathan, S.K. & Freedman, D.J. Preferential encoding of visual categories in parietal cortex compared with prefrontal cortex. Nat. Neurosci. 15, 315–320 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Merchant, H., Crowe, D.A., Robertson, M.S., Fortes, A.F. & Georgopoulos, A.P. Top-down spatial categorization signal from prefrontal to posterior parietal cortex in the primate. Front Syst. Neurosci 5, 69 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Goodwin, S.J., Blackman, R.K., Sakellaridi, S. & Chafee, M.V. Executive control over cognition: stronger and earlier rule-based modulation of spatial category signals in prefrontal cortex relative to parietal cortex. J. Neurosci. 32, 3499–3515 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Box, G.E.P., Jenkins, G.M. & Reinsel, G.C. Time Series Analysis: Forecasting and Control (Prentice-Hall, Upper Saddle River, New Jersey, USA, 1994).

  20. Granger, C.W.J. & Newbold, P. Forecasting Economic Time Series (Academic, New York, 1977).

  21. Christova, P., Lewis, S.M., Jerde, T.A., Lynch, J.K. & Georgopoulos, A.P. True associations between resting fMRI time series based on innovations. J. Neural Eng. 8, 046025 (2011).

    Article  CAS  PubMed  Google Scholar 

  22. Sugrue, L.P., Corrado, G.S. & Newsome, W.T. Matching behavior and the representation of value in the parietal cortex. Science 304, 1782–1787 (2004).

    Article  CAS  PubMed  Google Scholar 

  23. Gottlieb, J. & Balan, P. Attention as a decision in information space. Trends Cogn. Sci. 14, 240–248 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Peck, C.J., Jangraw, D.C., Suzuki, M., Efem, R. & Gottlieb, J. Reward modulates attention independently of action value in posterior parietal cortex. J. Neurosci. 29, 11182–11191 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Platt, M.L. & Glimcher, P.W. Neural correlates of decision variables in parietal cortex. Nature 400, 233–238 (1999).

    Article  CAS  PubMed  Google Scholar 

  26. Barraclough, D.J., Conroy, M.L. & Lee, D. Prefrontal cortex and decision making in a mixed-strategy game. Nat. Neurosci. 7, 404–410 (2004).

    Article  CAS  PubMed  Google Scholar 

  27. Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193–222 (1995).

    CAS  PubMed  Google Scholar 

  28. Fitzgerald, J.K. et al. Biased associative representations in parietal cortex. Neuron 77, 180–191 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Nee, D.E. & Brown, J.W. Dissociable frontal-striatal and frontal-parietal networks involved in updating hierarchical contexts in working memory. Cereb. Cortex 23, 2146–2158 (2013).

    Article  PubMed  Google Scholar 

  30. Gregoriou, G.G., Gotts, S.J., Zhou, H. & Desimone, R. High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324, 1207–1210 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Gregoriou, G.G., Gotts, S.J. & Desimone, R. Cell-type-specific synchronization of neural activity in FEF with V4 during attention. Neuron 73, 581–594 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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  PubMed  Google Scholar 

  33. Ferraina, S., Pare, M. & Wurtz, R.H. Comparison of cortico-cortical and cortico-collicular signals for the generation of saccadic eye movements. J. Neurophysiol. 87, 845–858 (2002).

    Article  PubMed  Google Scholar 

  34. Sherman, S.M. & Guillery, R.W. Distinct functions for direct and transthalamic corticocortical connections. J. Neurophysiol. 106, 1068–1077 (2011).

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank A. Georgopoulos for fundamental intellectual contributions to, and longstanding support of, this work. We thank P. Goldman-Rakic for critical insights into the network basis of prefrontal cortex function that strongly influenced this study. We thank D. Evans and D. Boeff for excellent technical assistance. We thank J. Ortiz and S. Te Nelson for assistance in training of nonhuman primates. Supported by the US National Institutes of Health (grant R01 MH077779 and R24MH069675), the Department of Veterans Affairs and the American Legion Brain Sciences Chair. R.K. Blackman was supported by US National Institutes of Health grant T32 GM008244. The views and opinions expressed in this work are those of the authors solely and not those of the United States Federal Government.

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Authors and Affiliations

  1. Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota, USA

    David A Crowe, Shikha J Goodwin, Rachael K Blackman & Matthew V Chafee

  2. Brain Sciences Center, Veterans Affairs Medical Center, Minneapolis, Minnesota, USA

    David A Crowe, Shikha J Goodwin, Rachael K Blackman, Sofia Sakellaridi, Scott R Sponheim & Matthew V Chafee

  3. Department of Biology, Augsburg College, Minneapolis, Minnesota, USA

    David A Crowe

  4. Medical Scientist Training Program (MD/PhD), University of Minnesota, Minneapolis, Minnesota, USA

    Rachael K Blackman

  5. Center for Cognitive Sciences, University of Minnesota, Minneapolis, Minnesota, USA

    Sofia Sakellaridi, Angus W MacDonald III & Matthew V Chafee

  6. Department of Psychiatry, University of Minnesota, Minneapolis, Minnesota, USA

    Scott R Sponheim & Angus W MacDonald III

  7. Department of Psychology, University of Minnesota, Minneapolis, Minnesota, USA

    Angus W MacDonald III

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Contributions

D.A.C. and M.V.C. analyzed the data and wrote the manuscript. S.J.G., R.K.B., S.S., S.R.S. and A.W.M. edited the manuscript. S.J.G. and M.V.C. designed the experiment, and S.R.S. and A.W.M. contributed to experimental design. S.J.G. trained the monkeys and collected the neural data. R.K.B., M.V.C. and S.S. assisted in neuronal data collection.

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Correspondence to Matthew V Chafee.

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Crowe, D., Goodwin, S., Blackman, R. et al. Prefrontal neurons transmit signals to parietal neurons that reflect executive control of cognition. Nat Neurosci 16, 1484–1491 (2013). https://doi.org/10.1038/nn.3509

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