Functional brain mapping during free viewing of natural scenes

Previous imaging studies have used mostly perceptually abstracted, idealized, or static stimuli to show segregation of function in the cerebral cortex. We wanted to learn whether functional segregation is maintained during more natural, complex, and dynamic conditions when many features have to be processed simultaneously, and identify regions whose activity correlates with the perception of specific features. To achieve this, we used functional magnetic resonance imaging (fMRI) to measure brain activity when human observers viewed freely dynamic natural scenes (a James Bond movie). The intensity with which they perceived different features (color, faces, language, and human bodies) was assessed psychometrically in separate sessions. In all subjects different features were perceived with a high degree of independence over time. We found that the perception of each feature correlated with activity in separate, specialized areas whose activity also varied independently. We conclude that even in natural conditions, when many features have to be processed simultaneously, functional specialization is preserved. Our method thus opens a new way of brain mapping, which allows the localization of a multitude of brain areas based on a single experiment using uncontrolled, natural stimuli. Furthermore, our results show that the intensity of activity in a specialized area is linearly correlated with the intensity of its perceptual experience. This leads us to suggest that each specialized area is directly responsible for the creation of a feature‐specific conscious percept (a microconsciousness). Hum. Brain Mapp. 21:75–83, 2004. © 2003 Wiley‐Liss, Inc.

[1]  P. Broca Perte de la parole, ramouissement chronique et destruction partielle du lobe antérieur gauche du cerveau , 1861 .

[2]  C. Wernicke Der aphasische Symptomenkomplex , 1974 .

[3]  S. Zeki Functional specialisation in the visual cortex of the rhesus monkey , 1978, Nature.

[4]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[5]  S. Zeki,et al.  A century of cerebral achromatopsia. , 1990, Brain : a journal of neurology.

[6]  A. Damasio,et al.  Face agnosia and the neural substrates of memory. , 1990, Annual review of neuroscience.

[7]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  S. Zeki,et al.  Cerebral akinetopsia (visual motion blindness). A review. , 1991, Brain : a journal of neurology.

[9]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  R. Turner,et al.  Characterizing Dynamic Brain Responses with fMRI: A Multivariate Approach , 1995, NeuroImage.

[11]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[12]  P. H. Schiller On the specificity of neurons and visual areas , 1996, Behavioural Brain Research.

[13]  E. Bullmore,et al.  Activation of auditory cortex during silent lipreading. , 1997, Science.

[14]  Karl J. Friston,et al.  Characterizing the Relationship between BOLD Contrast and Regional Cerebral Blood Flow Measurements by Varying the Stimulus Presentation Rate , 1997, NeuroImage.

[15]  S. Zeki,et al.  The position and topography of the human colour centre as revealed by functional magnetic resonance imaging. , 1997, Brain : a journal of neurology.

[16]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[17]  A. Dale,et al.  The Retinotopy of Visual Spatial Attention , 1998, Neuron.

[18]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

[19]  S. Zeki,et al.  The Riddoch syndrome: insights into the neurobiology of conscious vision. , 1998, Brain : a journal of neurology.

[20]  Semir Zeki,et al.  The theory of multistage integration in the visual brain , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[21]  T. Allison,et al.  Temporal Cortex Activation in Humans Viewing Eye and Mouth Movements , 1998, The Journal of Neuroscience.

[22]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[23]  S. Zeki,et al.  The asynchrony of consciousness , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[24]  S. Zeki,et al.  The cortical site for the generation of forms from motion , 1998, NeuroImage.

[25]  S. Zeki,et al.  Toward a Theory of Visual Consciousness , 1999, Consciousness and Cognition.

[26]  J. Haxby,et al.  Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects , 1999, Nature Neuroscience.

[27]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[28]  S Zeki,et al.  The clinical and functional measurement of cortical (in)activity in the visual brain, with special reference to the two subdivisions (V4 and V4 alpha) of the human colour centre. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  Jonathan E. Jennings,et al.  An fMRI version of the Farnsworth-Munsell 100-Hue test reveals multiple color-selective areas in human ventral occipitotemporal cortex. , 1999, Cerebral cortex.

[30]  J. Zihl,et al.  Cerebral Akinetopsia (Visual motion blindness). , 1999 .

[31]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

[32]  E. De Renzi Disorders of Visual Recognition , 2000, Seminars in neurology.

[33]  C. Frith,et al.  Unconscious activation of visual cortex in the damaged right hemisphere of a parietal patient with extinction. , 2000, Brain : a journal of neurology.

[34]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

[35]  S. Zeki,et al.  The architecture of the colour centre in the human visual brain: new results and a review * , 2000, The European journal of neuroscience.

[36]  M. Bar,et al.  Cortical Mechanisms Specific to Explicit Visual Object Recognition , 2001, Neuron.

[37]  J B Poline,et al.  Cerebral mechanisms of word masking and unconscious repetition priming , 2001, Nature Neuroscience.

[38]  Jeffrey M. Zacks,et al.  Human brain activity time-locked to perceptual event boundaries , 2001, Nature Neuroscience.

[39]  N. Kanwisher,et al.  A Cortical Area Selective for Visual Processing of the Human Body , 2001, Science.

[40]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[41]  M. Sereno,et al.  Mapping of Contralateral Space in Retinotopic Coordinates by a Parietal Cortical Area in Humans , 2001, Science.

[42]  F. Tong Brain at work: play by play , 2001, Nature Neuroscience.

[43]  S Zeki,et al.  The relationship between cortical activation and perception investigated with invisible stimuli , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Michael Erb,et al.  Object-selective responses in the human motion area MT/MST , 2002, Nature Neuroscience.

[45]  Alex R. Wade,et al.  Functional measurements of human ventral occipital cortex: retinotopy and colour. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[46]  Rafael Malach,et al.  Large-Scale Mirror-Symmetry Organization of Human Occipito-Temporal Object Areas , 2003, Neuron.

[47]  Andreas Bartels,et al.  The chronoarchitecture of the human brain: functional anatomy based on natural brain dynamics and on the principle of functional independence , 2004 .

[48]  D. Perrett,et al.  Visual neurones responsive to faces in the monkey temporal cortex , 2004, Experimental Brain Research.