Is there a dysexecutive syndrome?
Abstract
The role of the frontal lobes has often been described as a ‘paradox’ or a ‘riddle’. Ascribed to this region has been the loftiest of functions (e.g. executive; seat of wisdom); others contested that the frontal lobes played no special role. There has also been controversy about the unity or diversity of functions related to the frontal lobes. Based on the analysis of the effects of lesions of the frontal lobes, we propose that there are discrete categories of functions within the frontal lobes, of which ‘executive’ functioning is one. Within the executive category, the data do not support the concept of an undifferentiated central executive/supervisory system. The results are better explained as impairments in a collection of anatomically and functionally independent but interrelated attentional control processes. Evidence for three separate frontal attentional processes is presented. For each process, we present an operational description, the data supporting the distinctiveness of each process and the evidence for impairments of each process after lesions in specific frontal regions. These processes and their coarse frontal localizations are energization—superior medial, task setting—left lateral and monitoring—right lateral. The strength of the findings lies in replication: across different tasks; across different cognitive modalities (e.g. reaction time paradigms, memory); and across different patient groups. This convergence minimizes the possibility that any of the findings are limited to a specific task or to a specific set of patients. Although distinct, these processes are flexibly assembled in response to context, complexity and intention over real time into different networks within the frontal regions and between frontal and posterior regions.
References
Alexander M.P . 2001Chronic akinetic mutism after mesencephalic–diencephalic infarction: remediated with dopaminergic medications. Neurorehabil. Neural Repair. 15, 151–156. Crossref, PubMed, ISI, Google ScholarAlexander M.P . 2006Impairments of procedures for implementing complex language are due to disruption of frontal attention processes. J. Int. Neuropsychol. Soc. 12, 236–247. Crossref, PubMed, ISI, Google ScholarAlexander M.P, Stuss D.T& Fansabedian N . 2003California verbal learning test: performance by patients with focal frontal and non-frontal lesions. Brain. 126, 1493–1503.doi:10.1093/brain/awg128. . Crossref, PubMed, ISI, Google ScholarAlexander M.P, Stuss D.T, Shallice T, Picton T.W& Gillingham S . 2005Impaired concentration due to frontal lobe damage from two distinct lesion sites. Neurology. 65, 572–579.doi:10.1212/01.wnl.0000172912.07640.92. . Crossref, PubMed, ISI, Google Scholar- Alexander, M. P., Stuss, D. T., Picton, T., Shallice, T. & Gillingham, S. In press. Regional frontal injuries cause distinct forms of impaired attention to respond. Neurology. Google Scholar
Basso G, Nichelli P, Wharton C.M, Peterson M& Grafman J . 2003Distributed neural systems for temporal production: a functional MRI study. Brain Res. Bull. 59, 405–411.doi:10.1016/S0361-9230(02)00941-3. . Crossref, PubMed, ISI, Google ScholarBorkowski J.G, Benton A.L& Spreen O . 1967Word fluency and brain damage. Neuropsychologia. 5, 135–140.doi:10.1016/0028-3932(67)90015-2. . Crossref, ISI, Google ScholarBrass M& von Cramon D.Y . 2004Selection for cognitive control: a functional magnetic resonance imaging study on the selection of task-relevant information. J. Neurosci. 24, 8847–8852.doi:10.1523/JNEUROSCI.2513-04.2004. . Crossref, PubMed, ISI, Google ScholarBraver T.S, Barch D.M& Cohen J.D . 1999Cognition and control in schizophrenia: a computational model of dopamine and prefrontal function. Biol. Psychiatry. 46, 312–328.doi:10.1016/S0006-3223(99)00116-X. . Crossref, PubMed, ISI, Google ScholarBrutkowski S . 1965Functions of prefrontal cortex in animals. Physiol. Rev. 45, 721–746. Crossref, PubMed, ISI, Google ScholarBurgess P.W& Shallice T . 1994Fractionnement du syndrome frontal. Revue de Neuropsychologie. 4, 345–370. Google ScholarBurgess P.W& Shallice T . 1996Response suppression, initiation and strategy use following frontal lobe lesions. Neuropsychologia. 34, 263–272.doi:10.1016/0028-3932(95)00104-2. . Crossref, PubMed, ISI, Google ScholarBurgess P.W, Gilbert S.J& Dumontheil I . 2007Function and localization within rostral prefrontal cortex (area 10). Phil. Trans. R. Soc. B. 362, 887–899.doi:10.1098/rstb.2007.2095. . Link, ISI, Google ScholarCohen J.D, McClelland J.L& Dunbar K . 1990On the control of automatic processes: a parallel distributed processing account of the Stroop effect. Psychol. Rev. 97, 332–361.doi:10.1037/0033-295X.97.3.332. . Crossref, PubMed, ISI, Google ScholarComalli P.E, Wapner S& Werner H . 1962Interference effects of Stroop colour-word test in childhood, adulthood, and aging. J. Gen. Psychol. 100, 47–53. Crossref, ISI, Google ScholarCoull J.T, Frackowiak R.S& Frith C.D . 1998Monitoring for target objects: activation of right frontal and parietal cortices with increasing time on task. Neuropsychologia. 36, 1325–1334.doi:10.1016/S0028-3932(98)00035-9. . Crossref, PubMed, ISI, Google ScholarDelis D.C, Kramer J, Kaplan E& Ober B.A California verbal learning test (cvlt) manual. 1987San Antonio, TX:Psychological Corporation. Google ScholarDerfus J, Brass M, Neumann J& von Cramon D.Y . 2005Involvement of the inferior frontal junction in cognitive control: meta-analyses of switching and Stroop studies. Hum. Brain Mapp. 25, 22–34.doi:10.1002/hbm.20127. . Crossref, PubMed, ISI, Google ScholarDevinsky O, Morrell M& Vogt B.A . 1995Contributions of anterior cingulate cortex to behavior. Brain. 118, 279–306.doi:10.1093/brain/118.1.279. . Crossref, PubMed, ISI, Google ScholarDiaz R, Robbins T.W& Roberts A.C . 1996Dissociation in prefrontal cortex of affective attentional shifts. Nature. 380, 69–72.doi:10.1038/380069a0. . Crossref, PubMed, ISI, Google ScholarDrewe E.A An experimental investigation of luria's theory on the effects of frontal lobe lesions in man. Neuropsychologia. 13, 1975a421–429.doi:10.1016/0028-3932(75)90065-2. . Crossref, PubMed, ISI, Google ScholarDrewe E.A Go–no go learning after frontal lobe lesions in humans. Cortex. 11, 1975b8–16. Crossref, PubMed, Google ScholarDuncan J& Miller E.K Cognitive focus through adaptive neural coding in the primate prefrontal cortex. Principles of frontal lobe function, Stuss D.T& Knight R.T . 2002pp. 278–291. Eds. New York, NY:Oxford University Press. Crossref, Google ScholarElsass P& Hartelius H . 1985Reaction time and brain disease: relations to location, etiology and progression of cerebral dysfunction. Acta Neurol. Scand. 71, 11–19. Crossref, PubMed, ISI, Google ScholarFletcher P.C& Henson R.N . 2001Frontal lobes and human memory: insights from functional neuroimaging. Brain. 124, 849–881.doi:10.1093/brain/124.5.849. . Crossref, PubMed, ISI, Google ScholarGodefroy O, Lhullier C& Rousseaux M . 1994Vigilance and effects of fatigability, practice and motivation on simple reaction time tests in patients with lesion of the frontal lobe. Neuropsychologia. 32, 983–990.doi:10.1016/0028-3932(94)90047-7. . Crossref, PubMed, ISI, Google ScholarGodefroy O, Cabaret M, Petit-Chenal V, Pruvo J.-P& Rousseaux M . 1999Control functions of the frontal lobes. Modularity of the central-supervisory system?. Cortex. 35, 1–20. Crossref, PubMed, ISI, Google ScholarHeilman K.M& Watson R.T The neglect syndrome—a unilateral defect of the orienting response. Lateralization in the nervous system, Harnad S, Doty R.W, Jaynes J, Goldstein L& Krauthamer G . 1977pp. 285–302. Eds. New York, NY:Academic Press. Crossref, Google ScholarHenson R.N.A, Shallice T& Dolan R.J . 1999Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. Brain. 122, 1367–1381.doi:10.1093/brain/122.7.1367. . Crossref, PubMed, ISI, Google ScholarHockey G.R.J Cognitive energetic control mechanisms in the management of work demands and psychological health. Attention: selection, awareness and control. A tribute to Donald Broadbent, Baddeley A.D& Weiskrantz L . 1993pp. 328–345. Eds. Oxford, UK:Clarendon Press. Google ScholarHofle N, Paus T, Reutens D, Fiset P, Gotman J, Evans A.C& Jones B.E . 1997Regional cerebral blood flow changes as a function of delta and spindle activity during slow wave sleep in humans. J. Neurosci. 17, 4800–4808. Crossref, PubMed, ISI, Google ScholarIversen S.D& Mishkin M . 1970Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity. Exp. Brain Res. 11, 376–386.doi:10.1007/BF00237911. . Crossref, PubMed, ISI, Google ScholarKnight R.T Evoked potential studies of attention capacity in human frontal lobe lesions. Frontal lobe function and dysfunction, Levin H, Eisenberg H& Benton F . 1991pp. 139–153. Eds. New York, NY:Oxford University Press. Google ScholarKornblum S, Stevens G.T, Whipple A& Requin J . 1999The effects of irrelevant stimuli: 1. The time course of stimulus–stimulus and stimulus–response consistency effects with Stroop-like stimuli, Simon-like tasks, and their factorial combinations. J. Exp. Psychol. Hum. Percept. Perform. 25, 688–714.doi:10.1037/0096-1523.25.3.688. . Crossref, ISI, Google ScholarLeimkuhler M.E& Mesulam M.M . 1985Reversible go–no go deficits in a case of frontal lobe tumor. Ann. Neurol. 18, 617–619.doi:10.1002/ana.410180518. . Crossref, PubMed, ISI, Google ScholarLewis P.A& Miall R.C . 2003Brain activation patterns during measurement of sub- and supra-second intervals. Neuropsychologia. 41, 1583–1592.doi:10.1016/S0028-3932(03)00118-0. . Crossref, PubMed, ISI, Google ScholarLuria A.R The working brain: an introduction to neuropsychology. 1973New York, NY:Basic Books. Google ScholarLuu P, Collins P& Tucker D.M Mood, personality, and self-monitoring: negative affect and emotionality in relation to frontal lobe mechanisms of error monitoring. J. Exp. Psychol. Gen. 129, 2000a43–60.doi:10.1037/0096-3445.129.1.43. . Crossref, PubMed, ISI, Google ScholarLuu P, Flaisch T& Tucker D.M Medial frontal cortex in action monitoring. J. Neurosci. 20, 2000b464–469. Crossref, PubMed, ISI, Google ScholarMangels J.A, Ivry R.B& Shimizu N . 1998Dissociable contributions of the prefrontal and neocerebellar cortex to time perception. Cogn. Brain Res. 7, 15–39.doi:10.1016/S0926-6410(98)00005-6. . Crossref, PubMed, Google ScholarMilner B . 1963Effects of different brain lesions on card sorting: the role of the frontal lobes. Arch. Neurol. 9, 100–110. Crossref, Google ScholarNiemi P& Näätänen R . 1981Foreperiod and simple reaction time. Psychol. Bull. 89, 133–162.doi:10.1037/0033-2909.89.1.133. . Crossref, ISI, Google ScholarNorman D.A& Shallice T Attention to action: willed and automatic control of behaviour. Consciousness and self-regulation: advances in research and theory, Davidson R.J, Shwartz G.E& Shapiro D . 1986pp. 1–18. Eds. New York, NY:Plenum. Crossref, Google ScholarPardo J.V, Fox P.T& Raichle M.E . 1991Localization of a human system for sustained attention by positron emission tomography. Nature. 349, 61–64.doi:10.1038/349061a0. . Crossref, PubMed, ISI, Google ScholarPassingham R The frontal lobes and voluntary action. 1993Oxford, UK:Oxford University Press. Google ScholarPaus T . 2001Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat. Rev. Neurosci. 2, 417–424.doi:10.1038/35077500. . Crossref, PubMed, ISI, Google ScholarPaus T, Zatorre R.J, Hofle N, Caramanos J.G, Petrides M& Evans A.C . 1997Time-related changes in neural systems underlying attention and arousal during the performance of an auditory vigilance task. J. Cogn. Neurosci. 9, 392–408. Crossref, PubMed, ISI, Google ScholarPerret E . 1974Left frontal lobe of man and suppression of habitual responses in verbal categorical behavior. Neuropsychologia. 12, 323–330.doi:10.1016/0028-3932(74)90047-5. . Crossref, PubMed, ISI, Google ScholarPetrides M& Pandya D.M Comparative architectonic analysis of the human and macaque frontal cortex. Handbook of neuropsychology, Boller F& Grafman J . 1994pp. 17–57. Eds. Amsterdam, The Netherlands:Elsevier. Google ScholarPicard N& Strick P.L . 1996Motor areas of the medial wall: a review of their location and functional activation. Cereb. Cortex. 6, 342–353.doi:10.1093/cercor/6.3.342. . Crossref, PubMed, ISI, Google ScholarPicton T.W, Stuss D.T, Alexander M.P, Shallice T& Gillingham S . 2006Keeping time: Effects of focal frontal lesions. Neuropsychologia. 44, 1195–1209.doi:10.1016/j.neuropsychologia.2005.10.002. . Crossref, PubMed, ISI, Google Scholar- Picton, T. W., Stuss, D. T., Alexander, M. P., Shallice, T., Binns, M. A. & Gillingham, S. In press. Effects of focal frontal lesions on response inhibition. Cereb. Cortex. Google Scholar
Plum F& Posner J.B The diagnosis of stupor and coma. 3rd edn.1980Philadelphia, PA:Davis. Google ScholarPosner M.I& Petersen S.E . 1990The attention system of the human brain. Annu. Rev. Neurosci. 13, 25–42.doi:10.1146/annurev.ne.13.030190.000325. . Crossref, PubMed, ISI, Google ScholarRicher F, Decary A, Lapierre M.-P, Rouleau I, Bouvier G& Saint-Hilaire J.-M . 1993Target detection deficits in frontal lobectomy. Brain Cogn. 21, 203–211.doi:10.1006/brcg.1993.1016. . Crossref, PubMed, ISI, Google ScholarRobbins T.W . 1996Dissociating executive functions of the prefrontal cortex. Phil. Trans. R. Roc. B. 351, 1463–1470.doi:10.1098/rstb.1996.0131. . Link, ISI, Google ScholarRobbins T.W . 2007Shifting and stopping: fronto-striatal substrates, neurochemical modulation and clinical implications. Phil. Trans. R. Soc. B. 362, 917–932.doi:10.1098/rstb.2007.2097. . Link, ISI, Google ScholarRueckert L& Grafman J . 1996Sustained attention deficits in patients with right frontal lesions. Neuropsychologia. 34, 953–963.doi:10.1016/0028-3932(96)00016-4. . Crossref, PubMed, ISI, Google ScholarShallice T . 1982Specific impairments of planning. Phil. Trans. R. Soc. B. 298, 199–209.doi:10.1098/rstb.1982.0082. . Link, ISI, Google ScholarShallice T Fractionation of the supervisory system. Principles of frontal lobe function, Stuss D.T& Knight R.T . 2002pp. 261–277. Eds. New York, NY:Oxford University Press. Crossref, Google ScholarShallice T& Burgess P.W . 1991Deficits in strategy application following frontal lobe damage in man. Brain. 114, 727–741.doi:10.1093/brain/114.2.727. . Crossref, PubMed, ISI, Google ScholarStroop J.R . 1935Studies of interference in serial verbal reactions. J. Exp. Psychol. 18, 643–662.doi:10.1037/h0054651. . Crossref, Google ScholarSturm W& Willmes K . 2001On the functional neuroanatomy of intrinsic and phasic alertness. Neuroimage. 14, S76–S84.doi:10.1006/nimg.2001.0839. . Crossref, PubMed, ISI, Google ScholarStuss D.T . 2006Frontal lobes and attention: processes and networks, fractionation and integration. J. Int. Neuropsychol. Soc. 12, 261–271. Crossref, PubMed, ISI, Google ScholarStuss D.T New approaches to prefrontal lobe testing. The human frontal lobes: functions and disorders, Miller B& Cummings J 2nd edn2007pp. 292–305. Eds. New York, NY:Guildford Press. Google Scholar- Stuss, D. T. & Alexander, M. P. In press. Executive functions: is there a frontal lobe syndrome? In New encyclopedia of neuroscience. Google Scholar
Stuss D.T& Benson D.F . 1984Neuropsychological studies of the frontal lobes. Psychol. Bull. 95, 3–28.doi:10.1037/0033-2909.95.1.3. . Crossref, PubMed, ISI, Google ScholarStuss D.T& Levine B . 2002Adult clinical neuropsychology: lessons from studies of the frontal lobes. Annu. Rev. Psychol. 53, 401–433.doi:10.1146/annurev.psych.53.100901.135220. . Crossref, PubMed, ISI, Google ScholarStuss D.T, Stethem L.L, Hugenholtz H, Picton T.W, Pivik J& Richard M.T . 1989Reaction time after head injury: fatigue, divided and focused attention and consistency of performance. J. Neurol. Neurosurg. Psychiatry. 52, 742–748. Crossref, PubMed, ISI, Google ScholarStuss D.T, Alexander M.P, Palumbo C.L, Buckle L, Sayer L& Pogue J . 1994Organizational strategies of patients with unilateral or bilateral frontal lobe injury in word list learning tasks. Neuropsychology. 8, 355–373.doi:10.1037/0894-4105.8.3.355. . Crossref, Google ScholarStuss D.T, Shallice T, Alexander M.P& Picton T.W . 1995A multidisciplinary approach to anterior attentional functions. Ann. N. Y. Acad. Sci. 769, 191–211.doi:10.1111/j.1749-6632.1995.tb38140.x. . Crossref, PubMed, ISI, Google ScholarStuss D.T, Alexander M.P, Hamer L, Palumbo C, Dempster R, Binns M, Levine B& Izukawa D . 1998The effects of focal anterior and posterior brain lesions on verbal fluency. J. Int. Neuropsychol. Soc. 4, 265–278. Crossref, PubMed, ISI, Google ScholarStuss D.T, Toth J.P, Franchi D, Alexander M.P, Tipper S& Craik F.I.M . 1999Dissociation of attentional processes in patients with focal frontal and posterior lesions. Neuropsychologia. 37, 1005–1027.doi:10.1016/S0028-3932(98)00158-4. . Crossref, PubMed, ISI, Google ScholarStuss D.T, Levine B, Alexander M.P, Hong J, Palumbo C, Hamer L, Murphy K.J& Izukawa D . 2000Wisconsin card sorting test performance in patients with focal frontal and posterior brain damage: effects of lesion location and test structure on separable cognitive processes. Neuropsychologia. 38, 388–402.doi:10.1016/S0028-3932(99)00093-7. . Crossref, PubMed, ISI, Google ScholarStuss D.T, Floden D, Alexander M.P, Levine B& Katz D . 2001Stroop performance in focal lesion patients: dissociation of processes and frontal lobe lesion location. Neuropsychologia. 39, 771–786.doi:10.1016/S0028-3932(01)00013-6. . Crossref, PubMed, ISI, Google ScholarStuss D.T, Alexander M.P, Floden D.T, Binns M.A, Levine B, McIntosh A.R, Rajah M.N& Hevenor S.J Fractionation and localization of distinct frontal lobe processes: evidence from focal lesions in humans. Principles of frontal lobe function, Stuss D.T& Knight R.T . 2002app. 392–407. Eds. New York, NY:Oxford University Press. Crossref, Google ScholarStuss D.T, Binns M.A, Murphy K.J& Alexander M.P Dissociations within the anterior attentional system: effects of task complexity and irrelevant information on reaction time speed and accuracy. Neuropsychology. 16, 2002b500–513.doi:10.1037/0894-4105.16.4.500. . Crossref, PubMed, ISI, Google ScholarStuss D.T, Alexander M.P, Shallice T, Picton T.W, Binns M.A, MacDonald R, Borowiec A& Katz D . 2005Multiple frontal systems controlling response speed. Neuropsychologia. 43, 396–417.doi:10.1016/j.neuropsychologia.2004.06.010. . Crossref, PubMed, ISI, Google ScholarTalati A& Hirsch J . 2005Functional specialization within the medial frontal gyrus for perceptual go/no-go decisions based on “what,” “when,” and “where” related information: an fMRI study. J. Cogn. Neurosci. 17, 981–993.doi:10.1162/0898929054475226. . Crossref, PubMed, ISI, Google Scholar- Turner, M. S., Cipolotti, L., Yousry, T. & Shallice, T. In press. Qualitatively different memory impairments across frontal lobe subgroups. Neuropsychologia45, 1540–1552. (doi:10.1016/j.neuropsychologia.2006.11.013). Google Scholar
Vallesi A, Shallice T& Walsh V . 2007Role of the prefrontal cortex in the foreperiod effect. TMS evidence for dual mechanisms in temporal preparation. Cereb. Cortex. 17, 466–474.doi:10.1093/cercor/bhj163. . Crossref, PubMed, ISI, Google ScholarVerfaellie M& Heilman K.M . 1987Response preparation and response inhibition after lesions of the medial frontal lobe. Arch. Neurol. 44, 1265–1271. Crossref, PubMed, Google ScholarVuilleumier P& Driver J . 2007Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions. Phil. Trans. R. Soc. B. 362, 837–855.doi:10.1098/rstb.2007.2092. . Link, ISI, Google ScholarWest R& Baylis G.C . 1998Effects of increased response dominance and contextual disintegration on the Stroop interference effect in older adults. Psychol. Aging. 13, 206–217.doi:10.1037/0882-7974.13.2.206. . Crossref, PubMed, ISI, Google ScholarWilkins A.J, Shallice T& McCarthy R . 1987Frontal lesions and sustained attention. Neuropsychologia. 25, 359–365.doi:10.1016/0028-3932(87)90024-8. . Crossref, PubMed, ISI, Google Scholar


