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Top-down anticipatory control in prefrontal cortex

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Summary

The prefrontal cortex has been implicated in a wide variety of executive functions, many involving some form of anticipatory attention. Anticipatory attention involves the pre-selection of specific sensory circuits to allow fast and efficient stimulus processing and a subsequently fast and accurate response. It is generally agreed that the prefrontal cortex plays a critical role in anticipatory attention by exerting a facilitatory “top-down” bias on sensory pathways. In this paper we review recent results indicating that synchronized activity in prefrontal cortex, during anticipation of visual stimulus, can predict features of early visual stimulus processing and behavioral response. Although the mechanisms involved in anticipatory attention are still largely unknown, we argue that the synchronized oscillation in prefrontal cortex is a plausible candidate during sustained visual anticipation. We further propose a learning hypothesis that explains how this top-down anticipatory control in prefrontal cortex is learned based on accumulated prior experience by adopting a Temporal Difference learning algorithm.

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References

  • Arieli, A.; Sterkin, A.; Grinvald, A. and Aertsen, A. (1996) Dynamics of ongoing activity: Explanation of the large variability in evoked cortical responses. Science 273 (5283): 1868–1871.

    Article  PubMed  CAS  Google Scholar 

  • Baker, S. N.; Kilner, J. M.; Pinches, E. M. and Lemon, R. N. (1999) The role of synchrony and oscillations in the motor output. Exp. Brain Res. 128: 109–17.

    Article  PubMed  CAS  Google Scholar 

  • Basar, E.; Rahn, E.; Demiralp, T. and Schurmann, M. (1998) Spontaneous EEG theta activity controls frontal visual evoked potential amplitudes. Electroenceph. Clin. Neurophysiol. 108: 101–109.

    Article  PubMed  CAS  Google Scholar 

  • Berridge, K. C. and Robinson, T. E. (1998) What is the role of dopamine in reward: Hedonic impact, reward learning, or incentive salience? Brain Res. Rev. 28: 309–369.

    Article  PubMed  CAS  Google Scholar 

  • Brandt, M. E.; Jansen, B. H. and Carbonari, P. (1991) Pre-stimulus spectral EEG patterns and the visual evoked response. Electroenceph. Clin. Neurophysiol. 80: 16–20.

    Article  PubMed  CAS  Google Scholar 

  • Braver, T. S. and Cohen, J. D. (1999) Dopamine, cognitive control, and the gating model. In J. A. Reggia, E. Ruppin, & D. Glanzman (Eds.), Progress in brain research. Amsterdam: North-Holland: pp 327–349.

    Google Scholar 

  • Bressler, S. L. (1996) Interareal synchronization in the visual cortex. Behav. Brain Res. 76: 37–49.

    Article  PubMed  CAS  Google Scholar 

  • Bressler, S. L.; Coppola, R. and Nakamura, R. (1993) Episodic multiregional cortical coherence at multiple frequencies during visual task performance. Nature 366: 153–156.

    Article  PubMed  CAS  Google Scholar 

  • Bressler, S. L.; Liang, H. and Ding, M. (2001) Top-down influence on early visual processing by an anticipatory large-scale network in macaque prefrontal cortex. Soc. Neurosci. Abstr. 27, 533.1.

    Google Scholar 

  • Brown, L. L.; Schneider, J. S. and Lidsky, T. I. (1997) Sensory and cognitive functions of the basal ganglia. Curr. Opin. Neurobiol. 7: 157–163.

    Article  PubMed  CAS  Google Scholar 

  • Brunia, C. H. (1999) Neural aspects of anticipatory behavior. Acta. Psychol. 101: 213–42.

    Article  CAS  Google Scholar 

  • Chawla, D.; Rees, G. and Friston, K. J. (1999) The physiological basis of attentional modulation in extrastriate visual areas. Nat Neurosci. 2(7): 671–676.

    Article  PubMed  CAS  Google Scholar 

  • Chelazzi, L.; Miller, E. K.; Duncan, J. and Desimone, R. A (1993) neural basis for visual-search in inferior temporal cortex. Nature 363 (6427): 345–347.

    Article  PubMed  CAS  Google Scholar 

  • Church, R. M. (2002) Temporal learning. In R. Gallistel (Ed.), Stevens’ handbook of experimental psychology (Third edition): Learning, motivation, and emotion. New York: Wiley.

    Google Scholar 

  • Corbetta, M.; Kincade, J. M.; Ollinger, J. M.; McAvoy, M. P. and Shulman, G. L. (2000) Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat. Neurosci. 3(3): 292–297.

    Article  PubMed  CAS  Google Scholar 

  • Dayan, P. (2002) Reinforcement learning. In R. Gallistel (Ed.), Stevens’ handbook of experimental psychology (Third edition): Learning, motivation, and emotion. New York: Wiley.

    Google Scholar 

  • Dayan, P. and Abbott, L. F. (2001) Theoretical neuroscience. Cambridge, MA: MIT Press.

    Google Scholar 

  • De Oliveira, S. C.; Thiele, A.; Hoffmann, K. P. (1997) Synchronization of neuronal activity during stimulus expectation in a direction discrimination task. J. Neurosci. 17(23): 9248–9260.

    PubMed  Google Scholar 

  • Desimone, R. (1998) Visual attention mediated by biased competition in extrastriate visual cortex. Philos. Trans. Royal Soc. Lond. Series B-Biol. Sci. 353: 1245–1255.

    Article  CAS  Google Scholar 

  • Desimone, R. and Duncan, J. (1995) Neural mechanisms of selective visual-attention, Annu. Rev. Neurosci. 18: 193–222.

    Article  PubMed  CAS  Google Scholar 

  • Ding, M.; Bressler, S. L.; Yang, W. and Liang, H. (2000) Short window spectral analysis of cortical event-related potentials by Adaptive MultiVariate AutoRegressive (AMVAR) modeling: Data preprocessing, model validation, and variability assessment by bootstrapping. Biol Cybern 83: 35–45.

    Article  PubMed  CAS  Google Scholar 

  • Donoghue, J. P.; Sanes, J. N.; Hatsopoulos, N. G. and Gaal, G. (1998) Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. J. Neurophysiol. 97(1): 159–173.

    Google Scholar 

  • Driver, J.; Frith, C. (2000) Shifting baselines in attention research. Nat Rev Neurosci. 1: 147–148.

    Article  PubMed  CAS  Google Scholar 

  • Duncan, J.; Humphreys, G. and Ward, R. (1997) Competitive brain activity in visual attention. Curr. Opin. Neurobiol. 7: 255–261.

    Article  PubMed  CAS  Google Scholar 

  • Engel, A. K.; Fries, P. and Singer, W. (2001) Dynamic predictions: Oscillations and synchrony in top-down processing. Nat. Rev. Neurosci. 2(10): 704–716.

    Article  PubMed  CAS  Google Scholar 

  • Feige, B.; Aertsen, A. and Kristeva-Feige, R. (2000) Dynamic synchronization between multiple cortical motor areas and muscle activity in phasic voluntary movements. J. Neurophysiol. 84: 2622–9.

    PubMed  CAS  Google Scholar 

  • Felleman, D. and Van Essen, D. (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex. 1: 147.

    Article  Google Scholar 

  • Fries, P.; Reynolds, J. H.; Rorie, A. E. and Desimone, R. (2001) Modulation of oscillatory neuronal synchronization by selective visual attention, Science, 291: 1560–1563.

    Article  PubMed  CAS  Google Scholar 

  • Frith, C. (2001) A framework for studying the neural basis of attention. Neuropsychologia. 39: 1367–1371.

    Article  PubMed  CAS  Google Scholar 

  • Fuster, J. M. (2000) Executive frontal functions. Exp. Brain Res. 133: 66–70.

    Article  PubMed  CAS  Google Scholar 

  • Gehring, W. J.; Himle, J. and Nisenson, L. G. (2000) Action-monitoring deficits in obsessive-compulsive disorder. Psychol. Sci. 11: 1–6.

    Article  PubMed  CAS  Google Scholar 

  • Gilbert, C.; Ito, M.; Kapadia, M. and Westheimer, G. (2000) Interactions between attention, context and learning in primary visual cortex. Vision Res. 40: 1217–1226.

    Article  PubMed  CAS  Google Scholar 

  • Granger, C. W. J. (1969) Investigating causal relations by econometric models and cross-spectral methods. Econometrics 37: 424–438.

    Article  Google Scholar 

  • Gray, C. M. (1999) The temporal correlation hypothesis of visual feature integration: Still alive and well. Neuron 24(1): 31–47.

    Article  PubMed  CAS  Google Scholar 

  • Haig, A. R. and Gordon, E. (1998) Prestimulus EEG alpha phase synchronicity influences N100 amplitude and reaction time. Psychophysiol 35: 591–595.

    Article  CAS  Google Scholar 

  • Holroyd, C. B. and Coles, M. G. H. (2002) The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity. Psychol. Rev. 109: 679–709.

    Article  PubMed  Google Scholar 

  • Hopfinger, J. B.; Buonovore, M. H. and Mangun, G. R. (2000) The neural mechanisms of top-down attentional control. Nat Neurosci 3: 284–291.

    Article  PubMed  CAS  Google Scholar 

  • Kanwisher, N. and Wojciulik, E. (2000) Visual attention: Insights from brain imaging. Nat. Rev. Neurosci. 1(2): 91–100.

    Article  PubMed  CAS  Google Scholar 

  • Kastner, S.; Pinsk, M. A.; Weed, P. D.; Desimone, R. and Ungerleider, L. G. (1999) Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22: 751–761.

    Article  PubMed  CAS  Google Scholar 

  • Liang, H.; Ding, M.; Nakamura, R. and Bressler, S. L. (2000) Causal influence in primate cerebral cortex during visual pattern discrimination. NeuroReport 11: 2875–2880.

    Article  PubMed  CAS  Google Scholar 

  • Liang, H.; Bressler, S. L. Ding, M.; Truccolo, W. and Nakamura, R. (2002) Synchronized activity in prefrontal cortex during anticipation of visuomotor processing. NeuroReport 13: 2011–2015.

    Article  PubMed  Google Scholar 

  • Lutz, A.; Lachaux, J-P.; Martinerie, J. and Varela, F. J. (2002) Guiding the study of brain dynamics by using first-person data: Synchrony patterns correlate with ongoing conscious states during a simple visual task. Proc. Natl. Acad. Sci. USA 99: 1586–1591.

    Article  PubMed  CAS  Google Scholar 

  • Luck, S. J.; Chelazzi, L.; Hillyard, S. A. and Desimone, R. (1997) Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J. Neurophysiol. 77(1): 24–42.

    PubMed  CAS  Google Scholar 

  • Mackintosh, N. J. (1983) Conditioning and associative learning. Oxford: Oxford University Press.

    Google Scholar 

  • Makeig, S.; Westerfield, M.; Jung, T. P.; Enghoff, S.; Townsend, J.; Courchesne, E. and Sejnowski, T. J. (2002) Dynamic brain sources of visual evoked responses. Science 295 (5555): 690–694.

    Article  PubMed  CAS  Google Scholar 

  • Martinez, A.; Anllo-Vento, L.; Sereno, M. I.; Frank, L. R.; Buxton, R. B.; Dubowitz, D. J.; Wong, E. C.; Hinrichs, H.; Heinze, H. J. and Hillyard, S. A. (1999) Involvement of striate and extrastriate visual cortical areas in spatial attention. Nat. Neurosci. 2(4): 364–369.

    Article  PubMed  CAS  Google Scholar 

  • McCormick, D. A. (1990) Membrane properties and neurotransmitter actions. In: Shepard, G. M. (Eds) The Synaptic Organization of the Brain (3rd Ed.). New York: Oxford University Press.

    Google Scholar 

  • Miller, E. K. (2000) The prefrontal cortex and cognitive control. Nat. Rev. Neurosci. 1: 59–65.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Miller, K. D.; Chapman, B. and Stryker, M. P. (1989) Visual responses in adult cat visual cortex depend on N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. USA 86: 5183–5187.

    Article  PubMed  CAS  Google Scholar 

  • Miller, R. and Escobar, M. (2002) Learning: Laws and models of basic conditioning. In R. Gallistel (Ed.), Stevens’ handbook of experimental psychology (Third edition): Learning, motivation, and emotion. New York: Wiley.

    Google Scholar 

  • Monsell, S. and Driver, J. (2000) Control of Cognitive Processes. Cambridge, MA: MIT Press.

    Google Scholar 

  • Montague, P. R.; Dayan, P.; Sejnowski, T. K. (1996) A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J. Neurosci. 16: 1936–1947.

    PubMed  CAS  Google Scholar 

  • Mumford, D. (1994) Neuronal architectures for pattern-theoretic problems. In: Koch, C.; Davis, J. L. (Eds.) Large-Scale Neuronal Theories of the Brain. Cambridge, MA: MIT Press, pp 125–152.

    Google Scholar 

  • Niebur, E. (2002) Electrophysiological correlates of synchronous neural activity and attention: A short review. BioSystems 67: 157–166.

    Article  PubMed  Google Scholar 

  • Nobre, A. C. (2001) Orienting attention to instants in time. Neuropsychol. 39: 1317–1328.

    Article  CAS  Google Scholar 

  • O’Reilly, R. C. and Munakata, Y. (2000) Computational explorations in cognitive neuroscience. Cambridge, MA: MIT Press.

    Google Scholar 

  • Posner, M. I. and Dehaene, S. (2000) Attentional networks. In M. S. Gazzaniga (Ed.), Cognitive neuroscience: A reader. Malden, MA: Blackwell Publishers.

    Google Scholar 

  • Posner, M. I. and DiGirolamo, G. J. (1998) Executive attention: Conflict, target detection, and cognitive control. In R. Parasuraman (Ed.), The attentive brain. Cambridge, MA: MIT Press.

    Google Scholar 

  • Posner, M. I. and Petersen, S. E. (1990) The attention systems of the human brain. Ann. Rev. Neurosci. 13: 25–42.

    Article  PubMed  CAS  Google Scholar 

  • Poser, M. I. and Raichle, M. E. (1994) Images of mind. New York: Scientific American Library.

    Google Scholar 

  • Rescorla, R. A. and Wagner, A. R. (1972) A theory of Pavlovian conditioning: The effectiveness of reinforcement and non-reinforcement. In A. H. Black & W. F. Prokasy (Eds.), Classical conditioning II: Current research and theory. New York: Appleton-Century-Crofts.

    Google Scholar 

  • Ress, D.; Backus, B. and Heeger, D. (2000) Activity in primary visual cortex predicts performance in a visual detection task. Nat Neurosci. 3: 940–945.

    Article  PubMed  CAS  Google Scholar 

  • Reynolds, J.H.; Chelazzi, L. and Desimone, R. (1999) Competitive mechanisms subserve attention in macaque areas V2 and V4. J. Neurosci. 19: 1736–1753.

    PubMed  CAS  Google Scholar 

  • Riehle, A.; Grammont, F.; Diesmann, M. and Grun, S. (2000) Dynamical changes and temporal precision of synchronized spiking activity in monkey motor cortex during movement preparation. J. Physiol. (Paris) 94: 569–582.

    Article  CAS  Google Scholar 

  • Roelfsema, P. R.; Engel, A. K.; Konig, P. and Singer, W. (1997) Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385: 157–161.

    Article  PubMed  CAS  Google Scholar 

  • Schultz, W. (2000) Multiple reward signals in the brain. Nat Rev Neurosci 1: 199–207.

    Article  PubMed  CAS  Google Scholar 

  • Singer, W. and Gray, C. M. (1995) Visual feature integration and the temporal correlation hypothesis. Ann. Rev. Neurosci. 18: 555–586.

    Article  PubMed  CAS  Google Scholar 

  • Steinmetz, P. N.; Roy, A.; Fitzgerald, P. J.; Hsiao, S. S.; Johnson, K. O. and Niebur, E. (2000) Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature 404: 187–190.

    Article  PubMed  CAS  Google Scholar 

  • Sutton, R. S. (1988) Learning to predict by the methods of temporal differences. Mach. Learn. 3: 9–44.

    Google Scholar 

  • Sutton, R. S. and Barto, A. G. (1998) Reinforcement learning: An introduction. Cambridge, MA: MIT Press.

    Google Scholar 

  • Tononi, G.; Sporns, O. and Edelman, G. M. (1992) Reentry and the problem of integrating multiple cortical areas: simulation of dynamics integration in the visual system. Cereb Cortex 2: 310–335.

    Article  PubMed  CAS  Google Scholar 

  • Tsodyks, M.; Kenet, T.; Grinvald, A. and Arieli, A. (1999) Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286 (5446): 1943–1946.

    Article  PubMed  CAS  Google Scholar 

  • Ullman, S. (1995) Sequence seeking and counter streams: A computational model for bidirectional information flow in the visual cortex. Cereb. Cortex. 5: 1–11.

    Article  PubMed  CAS  Google Scholar 

  • Varela, F.; Lachaux, J-P.; Rodriguez, E. and Martinerie, J. (2001) The brainweb: phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2: 229–239.

    Article  PubMed  CAS  Google Scholar 

  • Von Stein, A.; Chiang, C. and Konig, P. (2000) Top-down processing mediated by interareal synchronization. Proc. Natl Acad. Sc. USA 97: 14748–14753.

    Article  Google Scholar 

  • Wickelgren, I. (1997) Getting the brain’s attention. Science, 278: 35–37.

    Article  PubMed  CAS  Google Scholar 

  • Zeki, S. (1993) A Vision of the Brain. Oxford: Blackwell Scientific.

    Google Scholar 

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  1. School of Health Information Sciences, University of Texas at Houston, 7000 Fannin St, Suite 600, 77030, Houston, TX, USA

    Hualou Liang & Hongbin Wang

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Liang, H., Wang, H. Top-down anticipatory control in prefrontal cortex. Theory Biosci. 122, 70–86 (2003). https://doi.org/10.1007/s12064-003-0038-7

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