Research Article
No access
Published Online: 15 January 2017

Greater Attention to Task-Relevant Threat Due to Orbitofrontal Lesion

Publication: Journal of Neurotrauma
Volume 34, Issue Number 2


Injury to the orbitofrontal cortex (OFC) is a frequent consequence of head injury and may lead to dysfunctional regulation of emotional and social behavior. Dysfunctional emotional behavior may partly be related to the role of the OFC in emotion-attention interaction, as reported previously. In order to better understand its role in emotion-attention and emotion-cognitive control interactions, we investigated attention allocation to task-relevant and task-irrelevant threat-related emotional stimuli during a task requiring cognitive control in patients with lesion to the OFC. We measured the behavioral performance and event-related potentials (ERP) of 13 patients with OFC lesion and 11 control subjects during a Go/NoGo visual discrimination task. In the task, line drawings of threatening (spider) and neutral (flower) figures served as either task-relevant Go or NoGo signals, or as task-irrelevant distractors. Overall performance did not differ between the groups. In contrast to the control group performance, the orbitofrontal group performance was improved by relevant threat signal in comparison with neutral signal. Further, task-relevant threat signals evoked larger frontocentral N2-P3 amplitude in the orbitofrontal group. Taken together, behavioral and electrophysiological results suggest that patients with OFC injury allocated more attentional and cognitive control resources in the context of task-relevant emotional stimuli. This study provides new evidence for the role of the OFC in emotion-attention and emotion-cognitive control interactions. Further, the OFC seems to contribute to the balance between voluntary and involuntary attention networks in context of emotional stimuli. Better understanding of alterations in emotion-attention interaction offers insight into affective dysfunction due to OFC lesion.

Get full access to this article

View all available purchase options and get full access to this article.


Hardman J.M., and Manoukian A. (2002). Pathology of head trauma. Neuroimaging Clin. N. Am. 12, 175–187.
Zald D.H., and Andreotti C. (2010). Neuropsychological assessment of the orbital and ventromedial prefrontal cortex. Neuropsychologia 48, 3377–3391.
Cicerone K.D., and Tanenbaum L.N. (1997). Disturbance of social cognition after traumatic orbitofrontal brain injury. Arch. Clin. Neuropsychol. 12, 173–188.
Angrilli A, Palomba D., Cantagallo A, Maietti A, and Stegagno L. (1999). Emotional impairment after right orbitofrontal lesion in a patient without cognitive deficits. Neuroreport 10, 1741–1746.
Beer J.S., John O.P., Scabini D., and Knight R.T. (2006). Orbitofrontal cortex and social behavior: integrating self-monitoring and emotion-cognition interactions. J. Cogn. Neurosci. 18, 871–879.
Bechara A. (2004). The role of emotion in decision-making: evidence from neurological patients with orbitofrontal damage. Brain Cogn. 55, 30–40.
Berlin H.A., Rolls E.T., and Kischka U. (2004). Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions. Brain 127, 1108–1126.
Stuss D.T. (2011). Traumatic brain injury: relation to executive dysfunction and the frontal lobes. Curr. Opin. Neurol. 24, 584–589.
Hartikainen K.M., Ogawa K.H., and Knight R.T. (2012). Orbitofrontal cortex biases attention to emotional events. J. Clin. Exp. Neuropsychol. 34, 588–597.
Horn N.R., Dolan M., Elliott R., Deakin J.F., and Woodruff P.W. (2003). Response inhibition and impulsivity: an fMRI study. Neuropsychologia 41, 1959–1966.
Bokura H., Yamaguchi S., and Kobayashi S. (2001). Electrophysiological correlates for response inhibition in a Go/NoGo task. Clin. Neurophysiol. 112, 2224–2232.
Beer J.S., Heerey E.A, Keltner D., Scabini D., and Knight R.T. (2003). The regulatory function of self-conscious emotion: insights from patients with orbitofrontal damage. J. Pers. Soc. Psychol. 85, 594–604.
Hornak J., Bramham J., Rolls E,T., Morris R.G., O'Doherty J., Bullock P.R., and Polkey C.E. (2003). Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. Brain 126, 1691–1712.
Bramham J., Morris R.G., Hornak J., Bullock P., and Polkey C.E. (2009). Social and emotional functioning following bilateral and unilateral neurosurgical prefrontal cortex lesions. J. Neuropsychol. 3, 125–143.
Bonelli R.M., and Cummings J.L. (2007). Frontal-subcortical circuitry and behavior. Dialogues Clin. Neurosci. 9, 141–151.
Szczepanski S.M., and Knight R.T. (2014). Insights into human behavior from lesions to the prefrontal cortex. Neuron 83, 1002–1018.
Diamond A. (2013). Executive functions. Annu. Rev. Psychol. 64, 135–168.
Desimone R., and Duncan J. (1995). Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193–222.
Desimone R. (1998). Visual attention mediated by biased competition in extrastriate visual cortex. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 353, 1245–1255.
Kastner S., and Ungerleider L.G. (2000). Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23, 315–341.
Hartikainen K.M., Ogawa K.H., and Knight R.T. (2000). Transient interference of right hemispheric function due to automatic emotional processing. Neuropsychologia 38, 1576–1580.
Hartikainen K.M., Ogawa K.H., Soltani M., and Knight R.T. (2007). Emotionally arousing stimuli compete for attention with left hemispace. Neuroreport 18, 1929–1933.
Papazacharias A., Taurisano P., Fazio L., Gelao B., Di Giorgio A., Lo Bianco L., Quarto T., Mancini M., Porcelli A., Romano R., Caforio G., Todarello O., Popolizio T., Blasi G., and Bertolino A. (2015). Aversive emotional interference impacts behavior and prefronto-striatal activity during increasing attentional control. Front. Behav. Neurosci. 9, 97.
Lobue V., and DeLoache J.S. (2008). Detecting the snake in the grass: attention to fear-relevant stimuli by adults and young children. Psychol. Sci. 19, 284–289.
Hartikainen K.M., Ogawa K.H., and Knight R.T. (2010). Trees over forest: unpleasant stimuli compete for attention with global features. Neuroreport 21, 344–348.
Hartikainen K.M., Siiskonen A.R., and Ogawa K.H. (2012). Threat interferes with response inhibition. Neuroreport 23, 447–450.
Sakaki M., Niki K., and Mather M. (2012). Beyond arousal and valence: the importance of the biological versus social relevance of emotional stimuli. Cogn. Affect. Behav. Neurosci. 12, 115–139.
Mäki-Marttunen V., Pickard N., Solbakk A.K., Ogawa K.H., Knight R.T., and Hartikainen K.M. (2014). Low attentional engagement makes attention network activity susceptible to emotional interference. Neuroreport 25, 1038–1043.
Oliveira L., Mocaiber I., David I.A., Erthal F., Volchan E., and Pereira M.G. (2013). Emotion and attention interaction: a trade-off between stimuli relevance, motivation and individual differences. Front. Hum. Neurosci. 7, 364.
Lavie N. (2005). Distracted and confused?: Selective attention under load. Trends Cogn. Sci. 9, 75–82.
Braver T.S., Cole M.W., and Yarkoni T. (2010). Vive les differences! Individual variation in neural mechanisms of executive control. Curr. Opin. Neurobiol. 20, 242–250.
Chen A.J., Britton M., Turner G.R., Vytlacil J., Thompson T.W., and D'Esposito M. (2012). Goal-directed attention alters the tuning of object-based representations in extrastriate cortex. Front. Hum. Neurosci. 6, 187.
Løvstad M., Funderud I., Lindgren M., Endestad T., Due-Tønnessen P., Meling T., Voytek B., Knight R.T., and Solbakk A.-K. (2011). Contribution of subregions of human frontal cortex to novelty processing. J. Cogn. Neurosci. 24, 378–395.
Rule R.R., Shimamura A.P., and Knight R.T. (2002). Orbitofrontal cortex and dynamic filtering of emotional stimuli. Cogn. Affect. Behav. Neurosci. 2, 264–270.
Hartikainen K.M., and Knight R. (2003). Lateral and orbital prefrontal cortex contributions to attention, in: Detection of Change: Event-Related Potential and fMRI Findings. Polich J. (ed). Kluwer Academic Press: The Netherlands, pps. 99–116.
Solbakk A.K., Reinvang I., Svebak S., Nielsen C.S., and Sundet K. (2005). Attention to affective pictures in closed head injury: event-related brain potentials and cardiac responses. J. Clin. Exp. Neuropsychol. 27, 205–223.
Solbakk A.K., and Løvstad M. (2014). Effects of focal prefrontal cortex lesions on electrophysiological indices of executive attention and action control. Scand. J. Psychol. 55, 233–243.
Mäki-Marttunen V., Kuusinen V., Brause M., Perakyla J., Polvivaara M., dos Santos Ribeiro R., Ohman J., and Hartikainen K.M. (2015). Enhanced attention capture by emotional stimuli in mild traumatic brain injury. J. Neurotrauma 32, 272–279.
Daffner K.R., Mesulam M.M., Scinto L.F., Cohen L.G., Kennedy B.P., West W.C., and Holcomb P.J. (1998). Regulation of attention to novel stimuli by frontal lobes: an event-related potential study. Neuroreport 9, 787–791.
Sun L., Perakyla J., Polvivaara M., Ohman J., Peltola J., Lehtimaki K., Huhtala H., and Hartikainen K.M. (2015). Human anterior thalamic nuclei are involved in emotion-attention interaction. Neuropsychologia 78, 88–94.
Daffner K.R., Scinto L.F., Calvo V., Faust R., Mesulam M.M., West W.C., and Holcomb P.J. (2000). The influence of stimulus deviance on electrophysiologic and behavioral responses to novel events. J. Cogn. Neurosci. 12, 393–406.
Vuilleumier P., and Schwartz S. (2001). Beware and be aware: capture of spatial attention by fear-related stimuli in neglect. Neuroreport 12, 1119–1122.
Liimatainen J., Peräkylä J., Järvelä K., Sisto T., Yli-Hankala A., and Hartikainen K.M. (2016). Improved cognitive flexibility after aortic valve replacement. Interact. J. Cardiovasc. Thorac. Surg. Epub ahead of print.
Hartikainen K.M., Waljas M., Isoviita T., Dastidar P., Liimatainen S., Solbakk A.K., Ogawa K.H., Soimakallio S., Ylinen A., and Ohman J. (2010). Persistent symptoms in mild to moderate traumatic brain injury associated with executive dysfunction. J. Clin. Exp. Neuropsychol. 32, 767–774.
Hartikainen K.M., Sun L., Polvivaara M., Brause M., Lehtimäki K., Haapasalo J., Möttönen T., Väyrynen K., Ogawa K.H., Öhman J., and Peltola J. (2014). Immediate effects of deep brain stimulation of anterior thalamic nuclei on executive functions and emotion-attention interaction in humans. J. Clin. Exp. Neuropsychol. 36, 540–550.
Brain Injuries (online). Current Care Guidelines. Working group set up by the Finnish Medical Society Duodecim, Finnish Neurological Society, Societas Medicinae Physicalis et Rehabilitationis Fenniae, Finnish Neurosurgical Society, Finnish Neuropsychological Society and Association of Finnish Insurance Medicine Doctors. Helsinki: The Finnish Medical Society Duodecim, 2008. Available at:
Rorden C., Karnath H.O., and Bonilha L. (2007). Improving lesion-symptom mapping. J. Cogn. Neurosci. 19, 1081–1088.
Roth R.M., Isquith P.K., Gioia G.A. (2005). Behavior Rating Inventory of Executive Function-Adult Version (BRIEF-A). Psychological Assessment Resources: Lutz, FL.
Beck A.T., Ward C.H., Mendelson M., Mock J., and Erbaugh J. (1961). An inventory for measuring depression. Arch. Gen. Psychiatry 4, 561–571.
King N.S., Crawford S., Wenden F.J., Moss N.E., and Wade D.T. (1995). The Rivermead Post Concussion Symptoms Questionnaire: a measure of symptoms commonly experienced after head injury and its reliability. J. Neurol. 242, 587–592.
Waid-Ebbs J.K., Wen P.S., Heaton S.C., Donovan N.J., and Velozo C. (2012). The item level psychometrics of the behaviour rating inventory of executive function-adult (BRIEF-A) in a TBI sample. Brain Inj. 26, 1546–1657.
Carretié L. (2014). Exogenous (automatic) attention to emotional stimuli: a review. Cogn. Affect. Behav. Neurosci. 14, 1228–1258.
Pessoa L. (2009). How do emotion and motivation direct executive control? Trends Cogn. Sci. 13, 160–166.
Jaeger T.F. (2008). Categorical data analysis: Away from ANOVAs (transformation or not) and towards logit mixed models. J. Mem. Lang. 59, 434–446.
Dixon P. (2008). Models of accuracy in repeated-measures designs. J. Mem. Lang. 59, 447–456.
R Core Team. (2015). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria.
Bates D.M. (2010). lme4: Mixed-Effects modeling with R. Springer: New York.
Wäljas M., Iverson G.L., Lange R.T., Hakulinen U., Dastidar P., Huhtala H., Liimatainen S., Hartikainen K., and Ohman J. (2015). A prospective biopsychosocial study of the persistent post-concussion symptoms following mild traumatic brain injury. J. Neurotrauma 32, 534–547.
Folstein J.R., and Van Petten C. (2008). Influence of cognitive control and mismatch on the N2 component of the ERP: a review. Psychophysiology 45, 152–170.
Padmala S., Bauer A., and Pessoa L. (2011). Negative emotion impairs conflict-driven executive control. Front. Psychol. 2, 192.
Bombardier C.H., Fann J.R., Temkin N.R., Esselman P.C., Barber J., and Dikmen S.S. (2010). Rates of major depressive disorder and clinical outcomes following traumatic brain injury. JAMA 303, 1938–1945.
Seidenberg M., Pulsipher D.T., and Hermann B. (2009). Association of epilepsy and comorbid conditions. Future Neurol. 4, 663–668.
Corbetta M., and Shulman G.L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215.
Anderson A.K., and Phelps E.A. (2001). Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 411, 305–309.
Öhman A. (2005). The role of the amygdala in human fear: automatic detection of threat. Psychoneuroendocrinology 30, 953–958.
Öhman A., Flykt A., and Esteves F. (2001). Emotion drives attention: detecting the snake in the grass. J. Exp. Psychol. Gen. 130, 466–478.
Shimamura A.P. (2000). The role of the prefrontal cortex in dynamic filtering. Psychobiology 28, 207–218.
Vossel S., Geng J.J., and Fink G.R. (2014). Dorsal and ventral attention systems: distinct neural circuits but collaborative roles. Neuroscientist 20, 150–159.
Chudasama Y., Passetti F., Rhodes S.E., Lopian D., Desai A., and Robbins T.W. (2003). Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: differential effects on selectivity, impulsivity and compulsivity. Behav. Brain Res. 146, 105–119.
Løvstad M., Funderud I., Endestad T., Due-Tønnessen P., Meling T.R., Lindgren M., Knight R.T., and Solbakk A.K. (2012). Executive functions after orbital or lateral prefrontal lesions: Neuropsychological profiles and self-reported executive functions in everyday living. Brain Inj. 26, 1586–1598.

Information & Authors


Published In

cover image Journal of Neurotrauma
Journal of Neurotrauma
Volume 34Issue Number 2January 15, 2017
Pages: 400 - 413
PubMed: 27502875


Published in print: January 15, 2017
Published online: 15 January 2017
Published ahead of print: 5 October 2016
Published ahead of production: 8 August 2016


Request permissions for this article.




    Verónica Mäki-Marttunen*
    Behavioral Neurology Research Unit, Department of Neurosciences and Rehabilitation, Tampere University Hospital, Tampere, Finland.
    CONICET, Buenos Aires, Argentina.
    Venla Kuusinen*
    Behavioral Neurology Research Unit, Department of Neurosciences and Rehabilitation, Tampere University Hospital, Tampere, Finland.
    Medical School, University of Tampere, Tampere, Finland.
    Jari Peräkylä
    Behavioral Neurology Research Unit, Department of Neurosciences and Rehabilitation, Tampere University Hospital, Tampere, Finland.
    Medical School, University of Tampere, Tampere, Finland.
    Keith H. Ogawa
    John Magaddino Neuroscience Laboratory, Saint Mary's College of California, Moraga, California.
    Maarja Brause
    Behavioral Neurology Research Unit, Department of Neurosciences and Rehabilitation, Tampere University Hospital, Tampere, Finland.
    Antti Brander
    Department of Radiology, Tampere University Hospital, Tampere, Finland.
    Kaisa M. Hartikainen
    Behavioral Neurology Research Unit, Department of Neurosciences and Rehabilitation, Tampere University Hospital, Tampere, Finland.
    Department of Neurology and Rehabilitation, Tampere University Hospital, Tampere, Finland.
    Medical School, University of Tampere, Tampere, Finland.


    Both authors contributed equally to this article.
    Address correspondence to:Kaisa M. HartikainenBehavioral Neurology Research UnitDepartment of Neurosciences and RehabilitationTampere University HospitalFinnmedi 6, 5th Floor, Biokatu 1433520 TampereFinland
    E-mail: [email protected]

    Author Disclosure Statement

    No competing financial interests exist.

    Metrics & Citations



    Export citation

    Select the format you want to export the citations of this publication.

    View Options

    Get Access

    Access content

    To read the fulltext, please use one of the options below to sign in or purchase access.

    Society Access

    If you are a member of a society that has access to this content please log in via your society website and then return to this publication.

    Restore your content access

    Enter your email address to restore your content access:

    Note: This functionality works only for purchases done as a guest. If you already have an account, log in to access the content to which you are entitled.

    View options


    View PDF/ePub

    Full Text

    View Full Text







    Copy the content Link

    Share on social media

    Back to Top