Parietal disruption impairs reflexive spatial attention within and between sensory modalities

Reflexive spatial attention is critical for controlling perception and action. An established body of evidence suggests that mechanisms of spatial attention operate both within and between sensory modalities; however the attentional mechanisms that link modalities in the human brain are unclear. Here we used transcranial magnetic stimulation (TMS) to explore the role of the parietal cortex in coordinating reflexive shifts of spatial attention between vision and touch. In two experiments, healthy participants localised visual and somatosensory targets that were preceded by non-informative visual or somatosensory spatial cues. To determine the role of parietal cortex in spatial orienting, TMS was delivered synchronously with cue onset for 100 ms. Results revealed a critical role of the right angular gyrus and supramarginal gyrus in reflexive orienting to visual and somatosensory targets that followed a somatosensory cue. In contrast, the same TMS protocol was ineffective in modulating reflexive orienting based on visual cues. This dependence on cue modality may reflect subcortical redundancy of visual orienting mechanisms. Overall, our results indicate a critical role of the inferior parietal cortex in mediating reflexive shifts of attention within and between sensory modalities.

[1]  B. Stein,et al.  The Merging of the Senses , 1993 .

[2]  S. Yantis,et al.  Transient neural activity in human parietal cortex during spatial attention shifts , 2002, Nature Neuroscience.

[3]  C. Spence,et al.  The Handbook of Multisensory Processing , 2004 .

[4]  T. Mondor,et al.  Facilitative and inhibitory effects of cuing sound duration, intensity, and timbre , 2001, Perception & psychophysics.

[5]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[6]  Jason B. Mattingley,et al.  Enhancement of visual selection during transient disruption of parietal cortex , 2006, Brain Research.

[7]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[8]  Sabine Kastner,et al.  Visual responses of the human superior colliculus: a high-resolution functional magnetic resonance imaging study. , 2005, Journal of neurophysiology.

[9]  C. Frith,et al.  Modulation of human visual cortex by crossmodal spatial attention. , 2000, Science.

[10]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[11]  D L Sparks,et al.  Effects of low-frequency stimulation of the superior colliculus on spontaneous and visually guided saccades. , 1993, Journal of neurophysiology.

[12]  Á. Pascual-Leone,et al.  Enhanced visual spatial attention ipsilateral to rTMS-induced 'virtual lesions' of human parietal cortex , 2001, Nature Neuroscience.

[13]  Francis McGlone,et al.  Reflexive spatial orienting of tactile attention , 2001, Experimental Brain Research.

[14]  A. Cowey,et al.  The role of the parietal cortex in visual attention—hemispheric asymmetries and the effects of learning: a magnetic stimulation study , 1998, Neuropsychologia.

[15]  Petroc Sumner,et al.  Signals Invisible to the Collicular and Magnocellular Pathways Can Capture Visual Attention , 2002, Current Biology.

[16]  Alan Cowey,et al.  Temporal aspects of visual search studied by transcranial magnetic stimulation , 1997, Neuropsychologia.

[17]  Katherine M. Armstrong,et al.  Visuomotor Origins of Covert Spatial Attention , 2003, Neuron.

[18]  C. Spence,et al.  On measuring selective attention to an expected sensory modality , 1997, Perception & psychophysics.

[19]  J. Assad,et al.  Neural coding of behavioral relevance in parietal cortex , 2003, Current Opinion in Neurobiology.

[20]  J. Mattingley,et al.  Parietal neglect and visual awareness , 1998, Nature Neuroscience.

[21]  C. Kennard,et al.  Distinct Cortical and Collicular Mechanisms of Inhibition of Return Revealed with S Cone Stimuli , 2004, Current Biology.

[22]  Scott T. Grafton,et al.  Involvement of visual cortex in tactile discrimination of orientation , 1999, Nature.

[23]  S. Petersen,et al.  Contributions of the pulvinar to visual spatial attention , 1987, Neuropsychologia.

[24]  U. Mosimann,et al.  Hemispheric asymmetry in visuospatial attention assessed with transcranial magnetic stimulation , 2002, Experimental Brain Research.

[25]  C. Spence,et al.  Visuo-tactile links in covert exogenous spatial attention remap across changes in unseen hand posture , 2002, Perception & psychophysics.

[26]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

[27]  Leslie G. Ungerleider,et al.  The neural basis of biased competition in human visual cortex , 2001, Neuropsychologia.

[28]  C. Spence,et al.  Cross-modal links in exogenous covert spatial orienting between touch, audition, and vision , 1998, Perception & psychophysics.

[29]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[30]  E. Macaluso,et al.  Multisensory spatial interactions: a window onto functional integration in the human brain , 2005, Trends in Neurosciences.

[31]  James R Müller,et al.  Microstimulation of the superior colliculus focuses attention without moving the eyes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Etienne Olivier,et al.  A Deficit in Covert Attention after Parietal Cortex Inactivation in the Monkey , 2004, Neuron.

[33]  Alan Cowey,et al.  Cortical plasticity in perceptual learning demonstrated by transcranial magnetic stimulation , 1998, Neuropsychologia.

[34]  J. Hoover,et al.  Divergent corticostriatal projections from a single cortical column in the somatosensory cortex of rats , 1998, Brain Research.

[35]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[36]  E. Macaluso,et al.  Supramodal Effects of Covert Spatial Orienting Triggered by Visual or Tactile Events , 2002, Journal of Cognitive Neuroscience.

[37]  Alexandre Pouget,et al.  A computational perspective on the neural basis of multisensory spatial representations , 2002, Nature Reviews Neuroscience.

[38]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[39]  Jason B. Mattingley,et al.  Modality-Specific Control of Strategic Spatial Attention in Parietal Cortex , 2004, Neuron.

[40]  J. Duncan,et al.  Competitive brain activity in visual attention , 1997, Current Opinion in Neurobiology.

[41]  J. Mattingley,et al.  Neurodisruption of selective attention: insights and implications , 2005, Trends in Cognitive Sciences.

[42]  S. Zeki,et al.  The neurology of saccades and covert shifts in spatial attention: an event-related fMRI study. , 2000, Brain : a journal of neurology.

[43]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[44]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[45]  K Sathian,et al.  Feeling with the mind's eye: contribution of visual cortex to tactile perception , 2002, Behavioural Brain Research.

[46]  Conrad V. Kufta,et al.  Attenuation in detection of somatosensory stimuli by transcranial magnetic stimulation. , 1991, Electroencephalography and clinical neurophysiology.

[47]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[48]  D L Robinson,et al.  Covert orienting of attention in macaques. III. Contributions of the superior colliculus. , 1995, Journal of neurophysiology.

[49]  Martin Eimer,et al.  Crossmodal links in spatial attention are mediated by supramodal control processes: evidence from event-related potentials. , 2002, Psychophysiology.

[50]  C. Spence,et al.  Tactile-Visual Links in Exogenous Spatial Attention under Different Postures: Convergent Evidence from Psychophysics and ERPs , 2001, Journal of Cognitive Neuroscience.

[51]  J. Mattingley,et al.  Fast and slow parietal pathways mediate spatial attention , 2004, Nature Neuroscience.