Modulation of the Contrast Response Function by Electrical Microstimulation of the Macaque Frontal Eye Field

Spatial attention influences representations in visual cortical areas as well as perception. Some models predict a contrast gain, whereas others a response or activity gain when attention is directed to a contrast-varying stimulus. Recent evidence has indicated that microstimulating the frontal eye field (FEF) can produce modulations of cortical area V4 neuronal firing rates that resemble spatial attention-like effects, and we have shown similar modulations of functional magnetic resonance imaging (fMRI) activity throughout the visual system. Here, we used fMRI in awake, fixating monkeys to first measure the response in 12 visual cortical areas to stimuli of varying luminance contrast. Next, we simultaneously microstimulated subregions of the FEF with movement fields that overlapped the stimulus locations and measured how microstimulation modulated these contrast response functions (CRFs) throughout visual cortex. In general, we found evidence for a nonproportional scaling of the CRF under these conditions, resembling a contrast gain effect. Representations of low-contrast stimuli were enhanced by stimulation of the FEF below the threshold needed to evoke saccades, whereas high-contrast stimuli were unaffected or in some areas even suppressed. Furthermore, we measured a characteristic spatial pattern of enhancement and suppression across the cortical surface, from which we propose a simple schematic of this contrast-dependent fMRI response.

[1]  W. Vanduffel,et al.  Visual Field Map Clusters in Macaque Extrastriate Visual Cortex , 2009, The Journal of Neuroscience.

[2]  Joonyeol Lee,et al.  A Normalization Model of Attentional Modulation of Single Unit Responses , 2009, PloS one.

[3]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

[4]  P. Roelfsema,et al.  Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex , 2008, Science.

[5]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[6]  Doris Y. Tsao,et al.  Patches with Links: A Unified System for Processing Faces in the Macaque Temporal Lobe , 2008, Science.

[7]  Barbara A Dosher,et al.  Blood oxygenation level-dependent contrast response functions identify mechanisms of covert attention in early visual areas , 2008, Proceedings of the National Academy of Sciences.

[8]  E. Seidemann,et al.  Linking Neuronal and Behavioral Performance in a Reaction-Time Visual Detection Task , 2007, The Journal of Neuroscience.

[9]  Tirin Moore,et al.  Rapid enhancement of visual cortical response discriminability by microstimulation of the frontal eye field , 2007, Proceedings of the National Academy of Sciences.

[10]  Giedrius T Buracas,et al.  The Effect of Spatial Attention on Contrast Response Functions in Human Visual Cortex , 2007, The Journal of Neuroscience.

[11]  Anna C Nobre,et al.  FEF TMS affects visual cortical activity. , 2006, Cerebral cortex.

[12]  M. Kenward,et al.  An Introduction to the Bootstrap , 2007 .

[13]  K. Obermayer,et al.  The Role of Feedback in Shaping the Extra-Classical Receptive Field of Cortical Neurons: A Recurrent Network Model , 2006, The Journal of Neuroscience.

[14]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

[15]  Juha Silvanto,et al.  Stimulation of the human frontal eye fields modulates sensitivity of extrastriate visual cortex. , 2006, Journal of neurophysiology.

[16]  John H. R. Maunsell,et al.  Effects of spatial attention on contrast response functions in macaque area V4. , 2006, Journal of neurophysiology.

[17]  Tirin Moore,et al.  Changes in Visual Receptive Fields with Microstimulation of Frontal Cortex , 2006, Neuron.

[18]  G. Orban,et al.  Charting the Lower Superior Temporal Region, a New Motion-Sensitive Region in Monkey Superior Temporal Sulcus , 2006, The Journal of Neuroscience.

[19]  Etienne Olivier,et al.  Contribution of the Monkey Frontal Eye Field to Covert Visual Attention , 2006, The Journal of Neuroscience.

[20]  E. J. Tehovnik,et al.  Mapping Cortical Activity Elicited with Electrical Microstimulation Using fMRI in the Macaque , 2005, Neuron.

[21]  Barry B. Lee,et al.  Psychophysics of electrical stimulation of striate cortex in macaques. , 2005, Journal of neurophysiology.

[22]  F. Hamker The reentry hypothesis: the putative interaction of the frontal eye field, ventrolateral prefrontal cortex, and areas V4, IT for attention and eye movement. , 2005, Cerebral cortex.

[23]  Robert H. Wurtz,et al.  Subcortical Modulation of Attention Counters Change Blindness , 2004, The Journal of Neuroscience.

[24]  Ji-Kyung Choi,et al.  Exogenous contrast agent improves sensitivity of gradient‐echo functional magnetic resonance imaging at 9.4 T , 2004, Magnetic resonance in medicine.

[25]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[26]  T. Moore,et al.  Microstimulation of the frontal eye field and its effects on covert spatial attention. , 2004, Journal of neurophysiology.

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

[28]  Olivier P. Faugeras,et al.  The Retinotopic Organization of Primate Dorsal V4 and Surrounding Areas: A Functional Magnetic Resonance Imaging Study in Awake Monkeys , 2003, The Journal of Neuroscience.

[29]  Katherine M. Armstrong,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2003, Nature.

[30]  Olivier D. Faugeras,et al.  Flows of diffeomorphisms for multimodal image registration , 2002, Proceedings IEEE International Symposium on Biomedical Imaging.

[31]  G. Orban,et al.  Extracting 3D from Motion: Differences in Human and Monkey Intraparietal Cortex , 2002, Science.

[32]  T. Paus,et al.  Transcranial Magnetic Stimulation of the Human Frontal Eye Field: Effects on Visual Perception and Attention , 2002, Journal of Cognitive Neuroscience.

[33]  S. Treue,et al.  Attentional Modulation Strength in Cortical Area MT Depends on Stimulus Contrast , 2002, Neuron.

[34]  Robin M Heidemann,et al.  Generalized autocalibrating partially parallel acquisitions (GRAPPA) , 2002, Magnetic resonance in medicine.

[35]  Anders M. Dale,et al.  Repeated fMRI Using Iron Oxide Contrast Agent in Awake, Behaving Macaques at 3 Tesla , 2002, NeuroImage.

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

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

[38]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

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

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

[41]  S. Nelson,et al.  Dynamics of neuronal processing in rat somatosensory cortex , 1999, Trends in Neurosciences.

[42]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

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

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

[45]  E. Todorov,et al.  A local circuit approach to understanding integration of long-range inputs in primary visual cortex. , 1998, Cerebral cortex.

[46]  M A Nicolelis,et al.  Nonlinear processing of tactile information in the thalamocortical loop. , 1997, Journal of neurophysiology.

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

[48]  G R Mangun,et al.  Spatial distribution of visual attention: Perceptual sensitivity and response latency , 1996, Perception & psychophysics.

[49]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[50]  Albert A. Michelson,et al.  Studies in Optics , 1995 .

[51]  J. Bullier,et al.  Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  R. Andersen,et al.  Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  C. Bruce,et al.  Topography of projections to posterior cortical areas from the macaque frontal eye fields , 1995, The Journal of comparative neurology.

[54]  G. Orban,et al.  Activity of inferior temporal neurons during orientation discrimination with successively presented gratings. , 1994, Journal of neurophysiology.

[55]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[56]  G W Humphreys,et al.  Luminance-increment detection: capacity-limited or not? , 1991, Journal of experimental psychology. Human perception and performance.

[57]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[58]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[59]  H. Hawkins,et al.  Visual attention modulates signal detectability. , 1990, Journal of experimental psychology. Human perception and performance.

[60]  Leslie G. Ungerleider,et al.  Pathways for motion analysis: Cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque , 1990, The Journal of comparative neurology.

[61]  W. Singer,et al.  Long-term recordings and receptive field measurements from single units of the visual cortex of awake unrestrained kittens , 1988, Journal of Neuroscience Methods.

[62]  G. Rizzolatti,et al.  Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention , 1987, Neuropsychologia.

[63]  M. Armstrong‐James,et al.  Spatiotemporal convergence and divergence in the rat S1 “Barrel” cortex , 1987, The Journal of comparative neurology.

[64]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[65]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[66]  Leslie G. Ungerleider,et al.  Cortical connections of visual area MT in the macaque , 1986, The Journal of comparative neurology.

[67]  Leslie G. Ungerleider,et al.  Projections to the superior temporal sulcus from the central and peripheral field representations of V1 and V2 , 1986, The Journal of comparative neurology.

[68]  C. Bruce,et al.  Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. , 1985, Journal of neurophysiology.

[69]  D. Simons Temporal and spatial integration in the rat SI vibrissa cortex. , 1985, Journal of neurophysiology.

[70]  D. G. Albrecht,et al.  Striate cortex of monkey and cat: contrast response function. , 1982, Journal of neurophysiology.

[71]  Howard S. Bashinski,et al.  Enhancement of perceptual sensitivity as the result of selectively attending to spatial locations , 1980, Perception & psychophysics.

[72]  Don McNicol,et al.  A Primer of Signal Detection Theory , 1976 .

[73]  K. Naka,et al.  S‐potentials from colour units in the retina of fish (Cyprinidae) , 1966, The Journal of physiology.