Spatial coding of visual and somatic sensory informationin body-centred coordinatesGaspare Galati, 1,3 Giorgia Committeri, 1,3 Jerome N. Sanes 2,4 * and Luigi Pizzamiglio 1,31 Laboratory of Neuropsychology, Fondazione Santa Lucia, via Ardeatina 306, Roma 00179, Italy2 Laboratory of Functional Neuroimaging, Fondazione Santa Lucia, Roma, Italy3 Department of Psychology, Universita` di Roma ‘La Sapienza’, Roma, Italy4 Department of Neuroscience, Brown Medical School, Providence, RI, USAKeywords: functional magnetic resonance imaging, humans, multimodal processing, sensory-motor transformations, spatialreference framesAbstractBecause sensory systems use different spatial coordinate frames, cross-modal sensory integration and sensory–motor coordinatetransformations must occur to build integrated spatial representations. Multimodal neurons using non-retinal body-centredreference frames are found in the posterior parietal and frontal cortices of monkeys. We used functional magnetic resonanceimaging to reveal regions of the human brain using body-centred coordinates to code the spatial position of both visual andsomatic sensory stimuli. Participants determined whether a visible vertical bar (visual modality) or a location touched by the rightindex finger (somatic sensory modality) lay to the left or to the right of their body mid-sagittal plane. This task was compared to aspatial control task having the same stimuli and motor responses and comparable difficulty, but not requiring body-centred codingof stimulus position. In both sensory modalities, the body-centred coding task activated a bilateral fronto-parietal network, thoughmore extensively in the right hemisphere, to include posterior parietal regions around the intraparietal sulcus and frontal regionsaround the precentral and superior frontal sulci, the inferior frontal gyrus and the superior frontal gyrus on the medial wall. Theoccipito-temporal junction and other extrastriate regions exhibited bilateral activation enhancement related to body-centred codingwhen driven by visual stimuli. We conclude that posterior parietal and frontal regions of humans, as in monkeys, appear toprovide multimodal integrated spatial representations in body-centred coordinates, and these data furnish the first indication ofsuch processing networks in the human brain.IntroductionSensory systems conveying spatial information to the brain usedifferent spatial coordinate frames. In order to build integrated spatialrepresentations and to plan accurate motor actions, cross-modalsensory integration and sensory–motor coordinate transformationsmustoccur. In monkeys, the parietal lobe appears tohavea crucial rolefor building and using such representations (Gross & Graziano, 1995;Rizzolatti et al., 1997; Colby & Goldberg, 1999), but direct andpersuasive evidence for comparable integrative processing in humanshas been lacking. Visual, auditory and tactile information converge inthe posterior parietal regions of monkeys where they becomesystematically combined with proprioceptive and vestibular cues soas to maintain constantly updated multimodal body-centred represen-tations of space (Andersen et al., 1997; Duhamel et al., 1992;Lacquanitietal.,1995).Parietalareashavedenseprojectionstofrontallobe areas devoted to motor control, including the premotor (PMA)and supplementary motor (SMA) areas and the frontal (FEF) andsupplementary (SEF) eye fields; and these projections probably relaytransformed and integrated spatial information to the frontal lobe.Frontal areas also respond to multimodal stimuli and encode spatiallocations in body-centred coordinates (Caminiti et al., 1991). Forexample, neurons in the ventral PMA respond to tactile stimulidelivered to the hand and to visual stimuli presented around the hand.Someofthesecellsshownonretinalvisualreceptivefields,anchoredtothe tactile receptive fields (Fogassi et al., 1996; Graziano et al., 1997).In humans, lesions to the parietal and frontal lobe, mainly to theright hemisphere, typically cause neglect for the contralesional sideof space (Vallar & Perani, 1986). This deficit occurs across sensorymodalities, and it is typically relative to body-centred referenceframes (Bisiach, 1997). Neuroimaging studies have also suggested animportant role for parieto-frontal structures in normal visual–motortransformations needed for reaching and adaptation to reversed vision(Lacquaniti et al., 1997; Sekiyama et al., 2000).Recent data suggest a role for posterior parietal and frontal corticalregions when humans code the position of visual stimuli relative tothe body midline (Vallar et al., 1999; Galati et al., 2000). Althoughthese studies revealed human brain networks that appear to constructbody-centred spatial codes using visual stimuli, only indirectevidence, that is, from lesion cases, exists to determine whetherparietal-frontal circuits in humans have a specific (that is, visuallydriven) or general (that is, multimodal) role in this coordinatetransformation process. Thus, the current work aimed to providedirect evidence on whether fronto-parietal networks in humans canCorrespondence: Dr Gaspare Galati,1 Laboratory of Neuropsychology, asabove.E-mail: gaspare.galati@uniroma1.it*Current address: Dr Jerome N. Sanes,4 Department of Neuroscience, asabove.Received 4 January 2001, revised 22 May 2001, accepted 18 June 2001European Journal of Neuroscience, Vol. 14, pp. 737–746, 2001 ª Federation of European Neuroscience Societies
