cortex 44 (2008) 109–118 available at www.sciencedirect.com journal homepage: www.elsevier.com/locate/cortex Research report Selective deficit of mental visual imagery with intact primary visual cortex and visual perception Valentina Moroa,*, Giovanni Berlucchib, Jason Lerchc, Francesco Tomaiuolod,e and Salvatore M. Agliotid,f,1 aDepartment of Psychology and Culture Anthropology, University of Verona, Italy bDepartment of Neurological and Visual Sciences, Physiology Section, University of Verona, Italy cBrain Imaging Centre, Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada dIRCCS Fondazione S. Lucia, Roma, Italy eAuxilium Vitae Volterra SpA, Volterra, Pisa, Italy fDepartment of Psychology, University of Rome ‘‘La Sapienza’’, Roma, Italy article info abstract Article history: There is a vigorous debate as to whether visual perception and imagery share the same Received 1 March 2006 neuronal networks, whether the primary visual cortex is necessarily involved in visual im- Reviewed 7 April 2006 agery, and whether visual imagery functions are lateralized in the brain. Two patients with Revised 6 June 2006 brain damage from closed head injury were submitted to tests of mental imagery in the Accepted 9 June 2006 visual, tactile, auditory, gustatory, olfactory and motor domains, as well as to an extensive Action editor Jane Riddoch testing of cognitive functions. A computerized mapping procedure was used to localize the Published online 17 November 2007 site and to assess the extent of the lesions. One patient showed pure visual mental imagery deficits in the absence of imagery deficits in other sensory domains as well as in the motor Keywords: domain, while the other patient showed both visual and tactile imagery deficits. Percep- Visual imagery and perception tual, language, and memory deficits were conspicuously absent. Computerized analysis V1 of the lesions showed a massive involvement of the left temporal lobe in both patients Higher order visual cortices and a bilateral parietal lesion in one patient. In both patients the calcarine cortex with Non-visual and motor imagery the primary visual area was bilaterally intact. Our study indicates that: (i) visual imagery Brain damaged patients deficits can occur independently from deficits of visual perception; (ii) visual imagery def- icits can occur when the primary visual cortex is intact and (iii) the left temporal lobe plays an important role in visual mental imagery. ª 2007 Elsevier Masson Srl. All rights reserved. 1. Introduction imagery. Visual mental images are assumed by some to be pic- ture-like or depictive in nature, that is representations which The definition of visual mental imagery as the process of ‘‘see- to a certain extent preserve the structural and spatial charac- ing with the mind’s eye’’ implies a close representational and teristics of the represented items. According to this assump- neural relationship between visual perception and visual tion, retinotopically organized cortical areas such as the * Corresponding author. Department of Psychology and Culture Anthropology, University of Verona, Lung. Porta Vittoria 17, 37122 Verona, VR, Italy. E-mail addresses: [email protected] (V. Moro), [email protected] (S.M. Aglioti). 1 Department of Psychology, University of Rome ‘‘La Sapienza’’, Via dei Marsi 78, 00185 Roma, Italy. 0010-9452/$ – see front matter ª 2007 Elsevier Masson Srl. All rights reserved. doi:10.1016/j.cortex.2006.06.004 110 cortex 44 (2008) 109–118 primary visual cortex can be similarly activated in a bottom- a hemorrhagic lesion in the middle and inferior temporal gy- up fashion by afferent pathways during perception and in rus of the left hemisphere. Patient 2 is a 23-year-old, right- a top-down fashion by back-projections from memory stores handed man employed as a factory worker. In a car accident during imagery (Kosslyn, 1987; Farah, 2001). A complete over- in 2000 he suffered a closed head injury with brain lesions in lap between the neural bases of visual perception and those of the left temporo-occipital area and the left medial and supe- visual imagery is, however, negated by the occurrence of rior parietal lobe. After the trauma both patients went into neurological syndromes whereby perception is impaired and a coma (Patient 1: Glasgow Coma Scale (GCS) ¼ 5, length of imagery is spared, or the reverse, although sparing of percep- coma ¼ 16 days; Patient 2: GCS ¼ 3, length of coma ¼ 14 tion in presence of a deranged imagery is seemingly never days). When they regained consciousness, they did not pres- complete (Farah, 2001; Bartolomeo, 2002). To account for ent any serious somatic or motor disabilities or signs of ideo- such double dissociations following brain damage, models motor or ideative apraxia. Initial difficulties in verbal memory, based on depictive representations have proposed that namely in word list learning tasks, cleared up in a few months. a shared system for perception and imagery may include spe- Language was preserved, even though Patient 2 showed some cialized components dedicated to one or the other function anomia and alexia with intact writing. Campimetric examina- (Behrmann et al., 1992). Yet other models claim that mental vi- tions showed no visual defects in Patient 2. In Patient 1 the sual images are propositional or descriptive in nature, so that first campimetric examination showed patches of reduced the brain does not have to re-enact a visual scene within the sensitivity in the right visual hemifield, greater in the lower head in order to imagine it. According to such models mental than the upper quadrant. These defects had disappeared 2 visual images do not require that a visuotopic pattern of neu- years after the accident, suggesting that they were most prob- ral activity be conjured up at some early station along the ably due to acute post-traumatic oedema. Nine months after visual pathways (Pylyshyn, 1973). These different views of the accident, both subjects were self-sufficient in daily activi- mental visual imagery are the object of current vigorous de- ties and able to return to their jobs. bates, but whichever model one favours, the quest for the Difficulties in visual mental imagery were reported during brain regions, which are involved in visual perception or interviews carried out 2 years (Patient 1) and 1 year (Patient 2) visual imagery or both is obviously of general interest for clin- after the brain damage. Patient 1, for example, reported her ical neurology and experimental neuropsychology alike. Evi- difficulty in ordering lunch or appetizers: ‘‘When they ask dence that is relevant to this issue comes from two main me if I want some crisps or peanuts, I’m unable to answer be- lines of research: the clinical consequences of localized brain cause I can’t mentally distinguish their different shapes’’. Cru- damage and the brain patterns of activation observed during cially, she was perfectly able to choose among crisps or visual performances in normal subjects. According to the first peanuts when they were presented visually. Patient 2 com- line of research, damage to the occipital lobe, which contains plained of his inability to draw when he did not have a model most of the retinotopic visual areas and is essential for normal to copy from. It is of interest that these complaints of both pa- visual perception, is neither necessary nor sufficient to pro- tients were limited to animals and objects, but did not involve duce visual imagery deficits. At least with regard to object familiar faces. Recognition of faces of relatives as well as of form and colour, imagery deficits are instead often observable persons encountered after the accident, such as rehabilitation after left temporal damage, independent of the presence or staff, was apparently intact. The subjects were submitted to absence of conspicuous visual perceptual deficits (Bartolo- general neuropsychological assessments in order to ascertain meo, 2002; Luzzatti et al., 1998; Trojano and Grossi, 1994). By the specific nature of these disorders. contrast, the second line of research has frequently, though not always, shown activations of occipital areas, down to 2.1. Neuropsychological assessment and including the primary visual cortex, along with many extra-occipital activations, during mental visual imagery in Each patient underwent a battery of tests assessing general normal subjects (Ganis et al., 2004; Mellet et al., 2000; Slotnick cognitive abilities, language, memory, and visuo-perceptual et al., 2005). abilities in four sessions carried out 2 years (Patient 1) and 1 The present report of two patients with brain damage from year (Patient 2) after the brain injury. closed head injury precisely localized with computerized General cognitive abilities were tested using the Weschler techniques is intended to contribute to the understanding of Adult Intelligence Scale-Revised (WAIS/R – Weschler, 1997) brain lesions leading to a very clear dissociation between and the Raven 48 Progressive Matrices Test (Raven, 1954). Pa- a normal visual perception and a severely defective visual im- tient 1’s scores were well within the normal limits (WAIS/R: agery. In both patients, this dissociation has occurred in the verbal ¼ 100, performance ¼ 95, Raven ¼ 53/60), while Patient presence of a completely intact visual cortex. Normal mental 2 showed a large difference between his verbal and perfor- imagery in non-visual sensory domains as well as in the mance scores, both of which, however, were still within motor domain