Skip to main content
SpringerLink
Log in

The prefrontal cortex and the executive control of attention

  • Review
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We review two studies aimed at understanding the role of prefrontal cortex (PFC) in the control of attention. The first study examined which attentional functions are critically dependent on PFC by removing PFC unilaterally and transecting the forebrain commissures in two macaques. The monkeys fixated a central cue and discriminated the orientation of a colored target grating presented among colored distracter gratings in either the hemifield affected by the PFC lesion or the normal control hemifield. When the cue was held constant for many trials, task performance in the affected hemifield was nearly normal. However, performance was severely impaired when the cue was switched frequently across trials. The monkeys were unimpaired in a pop-out task with changing targets that did not require top-down attentional control. Thus, the PFC lesion resulted in selective impairment in the monkeys’ ability to switch top-down control. In the second study, we used fMRI to investigate the neural correlates of top-down control in humans performing tasks identical to those used in the monkey experiments. Several fronto-parietal and posterior visual areas showed enhanced activation when attention was switched, which was greater on color cueing (top-down) trials relative to pop-out trials. Taken together, our findings indicate that both frontal and parietal cortices are involved in generating top-down control signals for attentive switching, which may then be fed back to visual processing areas. The PFC in particular plays a critical role in the ability to switch attentional control on the basis of changing task demands.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aron AR, Monsell S, Sahakian BJ, Robbins TW (2004) A componential analysis of task-switching deficits associated with lesions of left and right frontal cortex. Brain 127:1561–1573

    Article  PubMed  Google Scholar 

  • Asaad WF, Rainer G, Miller EK (1998) Neural activity in the primate prefrontal cortex during associative learning. Neuron 21:1399–1407

    Article  PubMed  CAS  Google Scholar 

  • Asaad WF, Rainer G, Miller EK (2000) Task-specific neural activity in the primate prefrontal cortex. J Neurophysiol 84:451–459

    PubMed  CAS  Google Scholar 

  • Barcelo F, Suwazono S, Knight RT (2000) Prefrontal modulation of visual processing in humans. Nat Neurosci 3:399–403

    Article  PubMed  CAS  Google Scholar 

  • Bianchi L (1922) The mechanism of the brain and the function of the frontal lobes. E. & S. Livingstone, Edinburgh

    Google Scholar 

  • Blasi V, Young AC, Tansy AP, Petersen SE, Snyder AZ, Corbetta M (2002) Word retrieval learning modulates right frontal cortex in patients with left frontal damage. Neuron 36:159–170

    Article  PubMed  CAS  Google Scholar 

  • Brass M, Ruge H, Meiran N, Rubin O, Koch I, Zysset S, Prinz W, von Cramon DY (2003) When the same response has different meanings: recoding the response meaning in the lateral prefrontal cortex. Neuroimage 20:1026–1031

    Article  PubMed  Google Scholar 

  • Braver TS, Reynolds JR, Donaldson DI (2003) Neural mechanisms of transient and sustained cognitive control during task switching. Neuron 39:713–726

    Article  PubMed  CAS  Google Scholar 

  • Bundesen C (1990) A theory of visual attention. Psychol Rev 97:523–547

    Article  PubMed  CAS  Google Scholar 

  • Bundesen C, Habekost T, Kyllingsbaek S (2005) A neural theory of visual attention: bridging cognition and neurophysiology. Psychol Rev 112:291–328

    Article  PubMed  Google Scholar 

  • Buschman TJ, Miller EK (2007) Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315:1860–1862

    Article  PubMed  CAS  Google Scholar 

  • Chao LL, Knight RT (1997) Prefrontal deficits in attention and inhibitory control with aging. Cereb Cortex 7:63–69

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dias R, Robbins TW, Roberts AC (1996a) Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380:69–72

    Article  PubMed  CAS  Google Scholar 

  • Dias R, Robbins TW, Roberts AC (1996b) Primate analogue of the Wisconsin Card Sorting Test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behav Neurosci 110:872–886

    Article  PubMed  CAS  Google Scholar 

  • Dosenbach NU, Fair DA, Cohen AL, Schlaggar BL, Petersen SE (2008) A dual-networks architecture of top-down control. Trends Cogn Sci 12:99–105

    Article  PubMed  Google Scholar 

  • Dove A, Pollmann S, Schubert T, Wiggins CJ, von Cramon DY (2000) Prefrontal cortex activation in task switching: an event-related fMRI study. Brain Res Cogn Brain Res 9:103–109

    Article  PubMed  CAS  Google Scholar 

  • Dreher JC, Berman KF (2002) Fractionating the neural substrate of cognitive control processes. Proc Natl Acad Sci USA 99:14595–14600

    Article  PubMed  CAS  Google Scholar 

  • Dreher JC, Grafman J (2003) Dissociating the roles of the rostral anterior cingulate and the lateral prefrontal cortices in performing two tasks simultaneously or successively. Cereb Cortex 13:329–339

    Article  PubMed  Google Scholar 

  • Dreher JC, Koechlin E, Ali SO, Grafman J (2002) The roles of timing and task order during task switching. Neuroimage 17:95–109

    Article  PubMed  Google Scholar 

  • Duncan J (1986) Disorganization of behaviour after frontal lobe damage. Cogn Neuropsychol 3:270–290

    Article  Google Scholar 

  • Ferrier D (1876) The functions of the brain. Smith Elder and Company, London

    Google Scholar 

  • Fuster JM (1995) Memory in the cerebral cortex. MIT Press, Cambridge

    Google Scholar 

  • Genovesio A, Brasted PJ, Mitz AR, Wise SP (2005) Prefrontal cortex activity related to abstract response strategies. Neuron 47:307–320

    Article  PubMed  CAS  Google Scholar 

  • Goldman-Rakic P (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In: Plum F (ed) Handbook of physiology: the nervous system. American Physiological Society, Bethesda, pp 373–417

    Google Scholar 

  • Grafman J (1994) Alternative frameworks for the conceptualization of prefrontal lobe functions. In: Boller FG, Grafman J (eds) Handbook of neuropsychology. Elsevier, Amsterdam, pp 187–202

    Google Scholar 

  • Grossberg S (1980) How does a brain build a cognitive code? Psychol Rev 87:1–51

    Article  PubMed  CAS  Google Scholar 

  • Hampshire A, Owen AM (2006) Fractionating attentional control using event-related fMRI. Cereb Cortex 16:1679–1689

    Article  PubMed  Google Scholar 

  • Hopfinger JB, Buonocore MH, Mangun GR (2000) The neural mechanisms of top-down attentional control. Nat Neurosci 3:284–291

    Article  PubMed  CAS  Google Scholar 

  • Hoshi E, Shima K, Tanji J (1998) Task-dependent selectivity of movement-related neuronal activity in the primate prefrontal cortex. J Neurophysiol 80:3392–3397

    PubMed  CAS  Google Scholar 

  • Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23:315–341

    Article  PubMed  CAS  Google Scholar 

  • Kastner S, Pinsk MA, De Weerd P, Desimone R, Ungerleider LG (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 

  • Knight RT (1984) Decreased response to novel stimuli after prefrontal lesions in man. Electroencephalogr Clin Neurophysiol 59:9–20

    Article  PubMed  CAS  Google Scholar 

  • Loose R, Kaufmann C, Tucha O, Auer DP, Lange KW (2006) Neural networks of response shifting: influence of task speed and stimulus material. Brain Res 1090:146–155

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Luria AR (1969) Frontal lobe syndromes. In: Vinken PJ, Bruyn GW (eds) Handbook of clinical neurology. Elsevier, New York, pp 725–757

    Google Scholar 

  • Manes F, Sahakian B, Clark L, Rogers R, Antoun N, Aitken M, Robbins T (2002) Decision-making processes following damage to the prefrontal cortex. Brain 125:624–639

    Article  PubMed  Google Scholar 

  • Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202

    Article  PubMed  CAS  Google Scholar 

  • Miller EK, Erickson CA, Desimone R (1996) Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J Neurosci 16:5154–5167

    PubMed  CAS  Google Scholar 

  • Milner B (1963) Effects of different brain lesions on card sorting. Arch Neurol 9:100–110

    Google Scholar 

  • Mishkin M (1964) Perseveration of central sets after frontal lesions in monkeys. In: Warren JM, Akert K (eds) The frontal granular cortex and behavior. McGraw-Hill, New York, pp 219–241

    Google Scholar 

  • Monchi O, Petrides M, Petre V, Worsley K, Dagher A (2001) Wisconsin Card Sorting revisited: distinct neural circuits participating in different stages of the task identified by event-related functional magnetic resonance imaging. J Neurosci 21:7733–7741

    PubMed  CAS  Google Scholar 

  • Moore T, Armstrong KM (2003) Selective gating of visual signals by microstimulation of frontal cortex. Nature 421:370–373

    Article  PubMed  CAS  Google Scholar 

  • Passingham R (1993) The frontal lobes and voluntary action. Oxford University Press, Oxford

    Google Scholar 

  • Pessoa L, Rossi A, Japee S, Desimone R, Ungerleider LG (2008) Attentional control during the transient updating of cue information. Brain Res (in press). Accessed 22 October 2008 [Epub]

  • Quintana J, Yajeya J, Fuster JM (1988) Prefrontal representation of stimulus attributes during delay tasks. I. Unit activity in cross-temporal integration of sensory and sensory-motor information. Brain Res 474:211–221

    Article  PubMed  CAS  Google Scholar 

  • Rainer G, Asaad WF, Miller EK (1998) Selective representation of relevant information by neurons in the primate prefrontal cortex. Nature 393:577–579

    Article  PubMed  CAS  Google Scholar 

  • Rossi AF, Bichot NP, Desimone R, Ungerleider LG (2007) Top down attentional deficits in macaques with lesions of lateral prefrontal cortex. J Neurosci 27:11306–11314

    Article  PubMed  CAS  Google Scholar 

  • Rushworth MF, Nixon PD, Eacott MJ, Passingham RE (1997) Ventral prefrontal cortex is not essential for working memory. J Neurosci 17:4829–4838

    PubMed  CAS  Google Scholar 

  • Schall JD (1997) Visuomotor areas of the frontal lobe. In: Rockland KS, Kaas JH, Peters A (eds) Cerebral cortex. Plenum Press, New York, pp 527–628

    Google Scholar 

  • Schall JD (2002) The neural selection and control of saccades by the frontal eye field. Philos Trans R Soc Lond B Biol Sci 357:1073–1082

    Article  PubMed  Google Scholar 

  • Shallice T, Burgess PW (1991) Deficits in strategy application following frontal lobe damage in man. Brain 114(Pt 2):727–741

    Article  PubMed  Google Scholar 

  • Slagter HA, Weissman DH, Giesbrecht B, Kenemans JL, Mangun GR, Kok A, Woldorff MG (2006) Brain regions activated by endogenous preparatory set shifting as revealed by fMRI. Cogn Affect Behav Neurosci 6:175–189

    Article  PubMed  CAS  Google Scholar 

  • Smith AB, Taylor E, Brammer M, Rubia K (2004) Neural correlates of switching set as measured in fast, event-related functional magnetic resonance imaging. Hum Brain Mapp 21:247–256

    Article  PubMed  Google Scholar 

  • Walker R, Husain M, Hodgson TL, Harrison J, Kennard C (1998) Saccadic eye movement and working memory deficits following damage to human prefrontal cortex. Neuropsychologia 36:1141–1159

    Article  PubMed  CAS  Google Scholar 

  • Wetherill GB, Levitt H (1965) Sequential estimation of points on a psychometric function. Br J Math Stat Psychol 18:1–10

    PubMed  CAS  Google Scholar 

  • White IM, Wise SP (1999) Rule-dependent neuronal activity in the prefrontal cortex. Exp Brain Res 126:315–335

    Article  PubMed  CAS  Google Scholar 

  • Yeung N, Nystrom LE, Aronson JA, Cohen JD (2006) Between-task competition and cognitive control in task switching. J Neurosci 26:1429–1438

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Neuroscience and Basic Behavioral Science, NIMH, NIH, Bethesda, MD, 20892, USA

    Andrew F. Rossi

  2. Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN, 47405, USA

    Luiz Pessoa

  3. McGovern Institute for Brain Research at MIT, Cambridge, MA, 02139, USA

    Robert Desimone

  4. Laboratory of Brain and Cognition, NIMH, NIH, Bethesda, MD, 20892, USA

    Leslie G. Ungerleider

Authors
  1. Andrew F. Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luiz Pessoa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert Desimone
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leslie G. Ungerleider
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Leslie G. Ungerleider.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rossi, A.F., Pessoa, L., Desimone, R. et al. The prefrontal cortex and the executive control of attention. Exp Brain Res 192, 489–497 (2009). https://doi.org/10.1007/s00221-008-1642-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-008-1642-z

Keywords

Search

Navigation