Attention-dependent suppression of metabolic activity in the early stages of the macaque visual system.

In this study we used a modified double-label deoxyglucose procedure to investigate attention-dependent modulations of deoxyglucose uptake at the earliest stages of the macaque visual system. Specifically, we compared activity levels evoked during two tasks with essentially identical visual stimulation requiring different attentional demands. During a featural-attention task, the subjects had to discriminate the orientation of a grating; during a control spatial-attention task, they had to localize the position of a target point. Comparison of the resulting activity maps revealed attention-dependent changes in metabolic activity in portions of the magnocellular layers of the lateral geniculate nucleus, and the magnocellular-recipient layers 4Calpha and 4B of the striate cortex. In these early stages of the visual system, attention to the orientation of the grating suppressed the metabolic activity in a retinotopically specific band peripheral to the representation of the stimulus. These results favor an early selection model of attention. After a thalamic attention-dependent gating mechanism, irrelevant visual information outside the focus of attention may be suppressed at the level of the striate cortex, which would then result in an increased signal-to-noise ratio for the processing of the attended feature in higher-tier, less retinotopically organized, extrastriate visual areas.

[1]  Barbara J. Winterson,et al.  Microsaccades during finely guided visuomotor tasks , 1976, Vision Research.

[2]  J. Malpeli,et al.  The representation of the visual field in the lateral geniculate nucleus of Macaca mulatta , 1975, The Journal of comparative neurology.

[3]  H. Jones,et al.  Context-dependent interactions and visual processing in V1 , 1996, Journal of Physiology-Paris.

[4]  D. V. van Essen,et al.  Responses in area V4 depend on the spatial relationship between stimulus and attention. , 1996, Journal of neurophysiology.

[5]  M. Corbetta,et al.  A PET study of visuospatial attention , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  B. C. Motter Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. , 1993, Journal of neurophysiology.

[7]  T. Brandt,et al.  Reciprocal inhibitory visual-vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex. , 1998, Brain : a journal of neurology.

[8]  J Nuyts,et al.  Different perceptual tasks performed with the same visual stimulus attribute activate different regions of the human brain: a positron emission tomography study. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[9]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[10]  G. Orban,et al.  The influence of stimulus location on the brain activation pattern in detection and orientation discrimination. A PET study of visual attention. , 1996, Brain : a journal of neurology.

[11]  R. W. Guillery,et al.  New views of the thalamic reticular nucleus in the adult and the developing brain , 1993, Trends in Neurosciences.

[12]  E. DeYoe,et al.  A physiological correlate of the 'spotlight' of visual attention , 1999, Nature Neuroscience.

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

[14]  T R Vidyasagar,et al.  Gating of neuronal responses in macaque primary visual cortex by an attentional spotlight , 1998, Neuroreport.

[15]  G. Caputo,et al.  Attentional selection by distractor suppression , 1998, Vision Research.

[16]  R Vogels,et al.  Human Brain Activity Related to Orientation Discrimination Tasks , 1997, The European journal of neuroscience.

[17]  M. Gazzaniga,et al.  Combined spatial and temporal imaging of brain activity during visual selective attention in humans , 1994, Nature.

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

[19]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[20]  Nikos K. Logothetis,et al.  Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex , 1998, Experimental Brain Research.

[21]  K. Cave,et al.  Flexibility in Spatial Attention Before and After Practice , 1997 .

[22]  N. Kanwisher,et al.  Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. , 1998, Journal of neurophysiology.

[23]  J. Maunsell,et al.  Effects of Attention on the Processing of Motion in Macaque Middle Temporal and Medial Superior Temporal Visual Cortical Areas , 1999, The Journal of Neuroscience.

[24]  A. Leventhal,et al.  Direction-sensitive X and Y cells within the A laminae of the cat's LGNd , 1994, Visual Neuroscience.

[25]  D. Hubel,et al.  Orientation columns in macaque monkey visual cortex demonstrated by the 2-deoxyglucose autoradiographic technique , 1977, Nature.

[26]  S. Sherman,et al.  Synaptic targets of thalamic reticular nucleus terminals in the visual thalamus of the cat , 2001, The Journal of comparative neurology.

[27]  M. Raichle,et al.  Blood flow changes in human somatosensory cortex during anticipated stimulation , 1995, Nature.

[28]  S. Miyauchi,et al.  Attention-regulated activity in human primary visual cortex. , 1998, Journal of neurophysiology.

[29]  T. Sejnowski,et al.  Computational Models of Thalamocortical Augmenting Responses , 1998, The Journal of Neuroscience.

[30]  Carrie J. McAdams,et al.  Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4 , 1999, The Journal of Neuroscience.

[31]  D. Heeger,et al.  Spatial attention affects brain activity in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[32]  G. Orban,et al.  Decision processes in visual discrimination of line orientation. , 1986, Journal of experimental psychology. Human perception and performance.

[33]  R. Desimone,et al.  Attention Increases Sensitivity of V4 Neurons , 2000, Neuron.

[34]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

[35]  C. Eriksen,et al.  Attentional distribution in the visual field duringsame-different judgments as assessed by response competition , 1993, Perception & psychophysics.

[36]  J. Chapin,et al.  Somatic sensory transmission to the cortex during movement: Phasic modulation over the locomotor step cycle , 1982, Experimental Neurology.

[37]  S. Hillyard,et al.  Involvement of striate and extrastriate visual cortical areas in spatial attention , 1999, Nature Neuroscience.

[38]  B. Bridgeman,et al.  The role of microsaccades in high acuity observational tasks , 1980, Vision Research.

[39]  J. Bourassa,et al.  Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer , 1995, Neuroscience.

[40]  V. M. Montero Amblyopia decreases activation of the corticogeniculate pathway and visual thalamic reticularis in attentive rats: a `focal attention' hypothesis , 1999, Neuroscience.

[41]  N. Logothetis,et al.  Functional imaging of the monkey brain , 1999, Nature Neuroscience.

[42]  D. Somers,et al.  Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[43]  G. Orban,et al.  Visual Motion Processing Investigated Using Contrast Agent-Enhanced fMRI in Awake Behaving Monkeys , 2001, Neuron.

[44]  G. Orban,et al.  How well do response changes of striate neurons signal differences in orientation: a study in the discriminating monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. I. Ocular dominance, binocular interactions, and baseline conditions , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  D. Hubel,et al.  Anatomy and physiology of a color system in the primate visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  John H. R. Maunsell,et al.  Attentional modulation of visual motion processing in cortical areas MT and MST , 1996, Nature.

[48]  D. Hubel,et al.  Effects of sleep and arousal on the processing of visual information in the cat , 1981, Nature.

[49]  E. G. Jones,et al.  The morphology of physiologically identified GABAergic neurons in the somatic sensory part of the thalamic reticular nucleus in the cat , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  G A Orban,et al.  Attention to One or Two Features in Left or Right Visual Field: A Positron Emission Tomography Study , 1997, The Journal of Neuroscience.

[51]  J H Maunsell,et al.  The Brain's Visual World: Representation of Visual Targets in Cerebral Cortex , 1995, Science.

[52]  A. A. Skavenski,et al.  Miniature eye movement. , 1973, Science.

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

[54]  M. Pinsk,et al.  Attention modulates responses in the human lateral geniculate nucleus , 2002, Nature Neuroscience.

[55]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. II. Retinotopic organization , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  L. H. Kronenberg Radioautography of multiple isotopes using color negative films. , 1979, Analytical biochemistry.

[57]  John K. Tsotsos Analyzing vision at the complexity level , 1990, Behavioral and Brain Sciences.

[58]  M. Posner,et al.  Attentional networks , 1994, Trends in Neurosciences.

[59]  D. Snodderly,et al.  Organization of striate cortex of alert, trained monkeys (Macaca fascicularis): ongoing activity, stimulus selectivity, and widths of receptive field activating regions. , 1995, Journal of neurophysiology.

[60]  S. Sherman,et al.  Dual response modes in lateral geniculate neurons: Mechanisms and functions , 1996, Visual Neuroscience.

[61]  D. V. van Essen,et al.  Spatial Attention Effects in Macaque Area V4 , 1997, The Journal of Neuroscience.

[62]  A H van der Heijden,et al.  Enhancing Single-Item Recognition Accuracy by Cueing Spatial Locations in Vision , 1985, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[63]  A. T. Smith,et al.  Attentional suppression of activity in the human visual cortex , 2000, Neuroreport.

[64]  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.

[65]  Alan C. Evans,et al.  Extraretinal modulation of cerebral blood flow in the human visual cortex: implications for saccadic suppression. , 1995, Journal of neurophysiology.

[66]  Sir G. Archaeopteryx Object-based attention in the primary visual cortex of the macaque monkey , 1998 .

[67]  D. Broadbent Perception and communication , 1958 .

[68]  Roger B. H. Tootell,et al.  Two methods for flat-mounting cortical tissue , 1985, Journal of Neuroscience Methods.

[69]  G. Mangun,et al.  ERP and fMRI measures of visual spatial selective attention , 1998, Human brain mapping.

[70]  M. Steriade,et al.  Reticularis thalami neurons revisited: activity changes during shifts in states of vigilance , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[71]  A. H. C. Heijden,et al.  The effects of advance location cueing on latencies in a single-letter recognition task , 1988, Psychological research.

[72]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[73]  B J Geesaman,et al.  Maps of complex motion selectivity in the superior temporal cortex of the alert macaque monkey: a double-label 2-deoxyglucose study. , 1997, Cerebral cortex.

[74]  E. Switkes,et al.  Deoxyglucose analysis of retinotopic organization in primate striate cortex. , 1982, Science.

[75]  Vivien A. Casagrande,et al.  The Afferent, Intrinsic, and Efferent Connections of Primary Visual Cortex in Primates , 1994 .

[76]  CJ Bruce,et al.  Resolution of metabolic columns by a double-label 2-DG technique: interdigitation and coincidence in visual cortical areas of the same monkey , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[77]  Eileen Kowler,et al.  Attentional interference at small spatial separations , 1999, Vision Research.

[78]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[79]  M. Reivich,et al.  Mapping of functional neural pathways by autoradiographic survey of local metabolic rate with (14C)deoxyglucose. , 1975, Science.

[80]  Alexander M. Harner,et al.  Task-dependent influences of attention on the activation of human primary visual cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[81]  Alan C. Evans,et al.  Double-label autoradiographic deoxyglucose method for sequential measurement of regional cerebral glucose utilization , 1987, Neuroscience.

[82]  J. Bullier,et al.  Visual latencies in areas V1 and V2 of the macaque monkey , 1995, Visual Neuroscience.

[83]  J. Wilson,et al.  Circuitry of the dorsal lateral geniculate nucleus in the cat and monkey. , 1993, Acta anatomica.

[84]  A. Treisman,et al.  Voluntary Attention Modulates fMRI Activity in Human MT–MST , 1997, Neuron.

[85]  W. Singer,et al.  A Metabolic Mapping Study of Orientation Discrimination and Detection Tasks in the Cat , 1997, The European journal of neuroscience.

[86]  F. Crick Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[87]  M. Reivich,et al.  THE [14C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT 1 , 1977, Journal of neurochemistry.

[88]  Richard S. J. Frackowiak,et al.  Functional localization of the system for visuospatial attention using positron emission tomography. , 1997, Brain : a journal of neurology.