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Brain Advance Access originally published online on June 4, 2003

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Brain, Vol. 126, No. 7, 1691-1712, July 2003
© 2003 Guarantors of Brain
doi: 10.1093/brain/awg168

Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices

J. Hornak¹, J. Bramham², E. T. Rolls¹, R. G. Morris², J. O’Doherty^1,3, P. R. Bullock⁴ and C. E. Polkey⁴

¹ University of Oxford, Department of Experimental Psychology, Oxford, ² Institute of Psychiatry, King’s College London, London, ³ Wellcome Department of Imaging Neuroscience, Institute of Neurology, Queen Square, London and ⁴ Academic Neurosurgery, Centre for Neuroscience Research, London, UK

Correspondence to: Professor E. T. Rolls, University of Oxford, Department of Experimental Psychology, South Parks Road, Oxford OX1 3UD, UK E-mail: edmund.rolls{at}psy.ox.ac.uk

To analyse the functions of different parts of the prefrontal cortex in emotion, patients with different prefrontal surgical excisions were compared on four measures of emotion: voice and face emotional expression identification, social behaviour, and the subjective experience of emotion. Some patients with bilateral lesions of the orbitofrontal cortex (OFC) had deficits in voice and face expression identification, and the group had impairments in social behaviour and significant changes in their subjective emotional state. Some patients with unilateral damage restricted to the OFC also had deficits in voice expression identification, and the group did not have significant changes in social behaviour or in their subjective emotional state. Patients with unilateral lesions of the antero-ventral part of the anterior cingulate cortex (ACC) and/or medial Brodmann area (BA) 9 were, in some cases, impaired on voice and face expression identification, had some change in social behaviour, and had significant changes in their subjective emotional state. Patients with unilateral lesions of the OFC and of the ACC and/or medial BA 9 were, in some cases, impaired on voice and face expression identification, had some changes in social behaviour, and had significant changes in their subjective emotional state. Patients with dorsolateral prefrontal cortex lesions or with medial lesions outside ACC and medial BA 9 areas (dorsolateral/other medial group) were unimpaired on any of these measures of emotion. In all cases in which voice expression identification was impaired, there were no deficits in control tests of the discrimination of unfamiliar voices and the recognition of environmental sounds. Thus bilateral or unilateral lesions circumscribed surgically within the OFC can impair emotional voice and/or face expression identification, but significant changes in social behaviour and in subjective emotional state are related to bilateral lesions. Importantly, unilateral lesions of the ACC (including some of medial BA 9) can produce voice and/or face expression identification deficits, and marked changes in subjective emotional state. These findings with surgically circumscribed lesions show that within the prefrontal cortex, both the OFC and the ACC/medial BA 9 region are involved in a number of aspects of emotion in humans including emotion identification, social behaviour and subjective emotional state, and that the dorsolateral prefrontal areas are not involved in emotion in these ways.

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