A backward progression of attentional effects in the ventral stream

The visual processing of behaviorally relevant stimuli is enhanced through top-down attentional feedback. One possibility is that feedback targets early visual areas first and the attentional enhancement builds up at progressively later stages of the visual hierarchy. An alternative possibility is that the feedback targets the higher-order areas first and the attentional effects are communicated “backward” to early visual areas. Here, we compared the magnitude and latency of attentional enhancement of firing rates in V1, V2, and V4 in the same animals performing the same task. We found a reverse order of attentional effects, such that attentional enhancement was larger and earlier in V4 and smaller and later in V1, with intermediate results in V2. These results suggest that attentional mechanisms operate via feedback from higher-order areas to lower-order ones.

[1]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

[2]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[3]  H. Kennedy,et al.  Topography of the afferent connectivity of area 17 in the macaque monkey: A double‐labelling study , 1986, The Journal of comparative neurology.

[4]  K. Rockland,et al.  Terminal arbors of individual “Feedback” axons projecting from area V2 to V1 in the macaque monkey: A study using immunohistochemistry of anterogradely transported Phaseolus vulgaris‐leucoagglutinin , 1989, The Journal of comparative neurology.

[5]  R. von der Heydt,et al.  Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  R. von der Heydt,et al.  Mechanisms of contour perception in monkey visual cortex. II. Contours bridging gaps , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Paul Antoine Salin,et al.  Projections from Areas 18 and 19 to Cat Striate Cortex: Divergence and Laminar Specificity , 1991, The European journal of neuroscience.

[8]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

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

[10]  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.

[11]  John Duncan,et al.  A neural basis for visual search in inferior temporal cortex , 1993, Nature.

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

[13]  P A Salin,et al.  Corticocortical connections in the visual system: structure and function. , 1995, Physiological reviews.

[14]  Shinsuke Shimojo,et al.  Visual surface representation: a critical link between lower-level and higher level vision , 1995 .

[15]  C. Gilbert,et al.  Improvement in visual sensitivity by changes in local context: Parallel studies in human observers and in V1 of alert monkeys , 1995, Neuron.

[16]  C. Gilbert,et al.  Spatial integration and cortical dynamics. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Victor A. F. Lamme,et al.  Contextual Modulation in Primary Visual Cortex , 1996, The Journal of Neuroscience.

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

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

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

[21]  Victor A. F. Lamme,et al.  Figure-ground activity in primary visual cortex is suppressed by anesthesia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[23]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[24]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[25]  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.

[26]  C. Gilbert,et al.  Attention Modulates Contextual Influences in the Primary Visual Cortex of Alert Monkeys , 1999, Neuron.

[27]  Z Li,et al.  Visual segmentation by contextual influences via intra-cortical interactions in the primary visual cortex. , 1999, Network.

[28]  Heiko Neumann,et al.  Recurrent V1–V2 interaction in early visual boundary processing , 1999, Biological Cybernetics.

[29]  Leslie G. Ungerleider,et al.  Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys , 2000, Nature Neuroscience.

[30]  Victor A. F. Lamme,et al.  Separate processing dynamics for texture elements, boundaries and surfaces in primary visual cortex of the macaque monkey. , 1999, Cerebral cortex.

[31]  R. von der Heydt,et al.  Coding of Border Ownership in Monkey Visual Cortex , 2000, The Journal of Neuroscience.

[32]  G A Orban,et al.  Attention-dependent suppression of metabolic activity in the early stages of the macaque visual system. , 2000, Cerebral cortex.

[33]  C. Schroeder,et al.  Intermodal selective attention in monkeys. I: distribution and timing of effects across visual areas. , 2000, Cerebral cortex.

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

[35]  J. Bakin,et al.  Visual Responses in Monkey Areas V1 and V2 to Three-Dimensional Surface Configurations , 2000, The Journal of Neuroscience.

[36]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

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

[38]  Shaul Hochstein,et al.  The spread of attention and learning in feature search: effects of target distribution and task difficulty , 2000, Vision Research.

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

[40]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[41]  T. S. Lee,et al.  Dynamics of subjective contour formation in the early visual cortex. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[42]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[43]  Leslie G. Ungerleider,et al.  Contextual Modulation in Primary Visual Cortex of Macaques , 2001, The Journal of Neuroscience.

[44]  P Girard,et al.  Feedback connections act on the early part of the responses in monkey visual cortex. , 2001, Journal of neurophysiology.

[45]  Richard B Buxton,et al.  Putting spatial attention on the map: timing and localization of stimulus selection processes in striate and extrastriate visual areas , 2001, Vision Research.

[46]  H. Spekreijse,et al.  Two distinct modes of sensory processing observed in monkey primary visual cortex (V1) , 2001, Nature Neuroscience.

[47]  J. Bullier,et al.  Feedforward and feedback connections between areas V1 and V2 of the monkey have similar rapid conduction velocities. , 2001, Journal of neurophysiology.

[48]  J. Driver,et al.  Segmentation, attention and phenomenal visual objects , 2001, Cognition.

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

[50]  S. Hochstein,et al.  View from the Top Hierarchies and Reverse Hierarchies in the Visual System , 2002, Neuron.

[51]  D. V. van Essen,et al.  Scene segmentation and attention in primate cortical areas V1 and V2. , 2002, Journal of neurophysiology.

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

[53]  Alexander Grunewald,et al.  Neural Correlates of Structure-from-Motion Perception in Macaque V1 and MT , 2002, The Journal of Neuroscience.

[54]  Lin Chen.  The topological approach to perceptual organization , 2005 .

[55]  R. Reid,et al.  Attention Modulates the Responses of Simple Cells in Monkey Primary Visual Cortex , 2005, The Journal of Neuroscience.

[56]  Robert Desimone,et al.  Impaired filtering of distracter stimuli by TE neurons following V4 and TEO lesions in macaques. , 2004, Cerebral cortex.

[57]  Rainer Goebel,et al.  Receptive field size-dependent attention effects in simultaneously presented stimulus displays , 2006, NeuroImage.

[58]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[59]  Daniel Yoshor,et al.  Spatial Attention Does Not Strongly Modulate Neuronal Responses in Early Human Visual Cortex , 2007, The Journal of Neuroscience.

[60]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[61]  R. Wurtz,et al.  Guarding the gateway to cortex: attention in visual thalamus , 2008, Nature.

[62]  R. Desimone,et al.  The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4 , 2008, The Journal of Neuroscience.

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

[64]  Junying Yuan,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2022 .