Cortical Response to Task-relevant Stimuli Presented outside the Primary Focus of Attention

Visual attention selectively enhances the neural response to a task-relevant item. But what happens when an item outside the primary focus of attention is also relevant to the task at hand? In a dual-task fMRI experiment, we studied the responses in retinotopically organized visual cortex in such a situation. Observers performed an attention-demanding task in the fovea while another, unmasked stimulus appeared in the visual periphery. With respect to this latter stimulus, observers attempted to perform either a less or a more attentionally demanding task. Both tasks increased the BOLD response to the peripheral stimulus. Behaviorally, however, only the less demanding task was performed well, whereas the demanding task was carried out near chance. What could explain the discrepancy between BOLD response and behavioral performance? A control experiment revealed that the report of the less demanding feature was severely disturbed by a mask. Moreover, the visual attributes queried by the demanding task had a significantly shorter iconic memory persistence. We conclude that, in the dual-task situation, the focus of attention initially remains with the foveal task, but subsequently shifts to the former location of the peripheral stimulus. Such a belated shift to a peripheral iconic memory (futile in one case, informative in the other) would reconcile the similar BOLD response with the disparate behavioral performance. In summary, our results show that an enhanced BOLD response is consistently associated with attentional modulation, but not with behavioral performance.

[1]  Kenji Kawano,et al.  Global and fine information coded by single neurons in the temporal visual cortex , 1999, Nature.

[2]  Leila Reddy,et al.  Face-gender discrimination is possible in the near-absence of attention. , 2004, Journal of vision.

[3]  Sabine Kastner,et al.  Visual attention as a multilevel selection process , 2004, Cognitive, affective & behavioral neuroscience.

[4]  P. Maquet,et al.  Orienting Attention to Locations in Perceptual Versus Mental Representations , 2004, Journal of Cognitive Neuroscience.

[5]  Tomaso Poggio,et al.  Fast Readout of Object Identity from Macaque Inferior Temporal Cortex , 2005, Science.

[6]  J. Braun,et al.  Perceptual reversals need no prompting by attention. , 2007, Journal of vision.

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

[8]  C D Frith,et al.  Modulating irrelevant motion perception by varying attentional load in an unrelated task. , 1997, Science.

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

[10]  M. D’Esposito,et al.  The neural basis of the central executive system of working memory , 1995, Nature.

[11]  D. Sagi,et al.  Vision outside the focus of attention , 1990, Perception & psychophysics.

[12]  D. Perrett,et al.  Time course of neural responses discriminating different views of the face and head. , 1992, Journal of neurophysiology.

[13]  Guillaume A. Rousselet,et al.  Parallel processing in high-level categorization of natural images , 2002, Nature Neuroscience.

[14]  Alexander Pastukhov,et al.  Visual attention is a single, integrated resource , 2009, Vision Research.

[15]  C. Koch,et al.  Visual Search and Dual Tasks Reveal Two Distinct Attentional Resources , 2004, Journal of Cognitive Neuroscience.

[16]  Joel L. Davis,et al.  Visual attention and cortical circuits , 2001 .

[17]  A. Nobre,et al.  Attentional modulation of object representations in working memory. , 2007, Cerebral cortex.

[18]  D. Heeger,et al.  Activity in primary visual cortex predicts performance in a visual detection task , 2000, Nature Neuroscience.

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

[20]  P. Perona,et al.  Rapid natural scene categorization in the near absence of attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[21]  B Giesbrecht,et al.  Neural mechanisms of top-down control during spatial and feature attention , 2003, NeuroImage.

[22]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[23]  G. Rousselet,et al.  Is it an animal? Is it a human face? Fast processing in upright and inverted natural scenes. , 2003, Journal of vision.

[24]  Christof Koch,et al.  Attentional capacity is undifferentiated: Concurrent discrimination of form, color, and motion , 1999, Perception & psychophysics.

[25]  C. Koch,et al.  Attention and consciousness: two distinct brain processes , 2007, Trends in Cognitive Sciences.

[26]  Árni Kristjánsson,et al.  Readout From Iconic Memory and Selective Spatial Attention Involve Similar Neural Processes , 2007, Psychological science.

[27]  G. Woodman,et al.  Neural fate of ignored stimuli: dissociable effects of perceptual and working memory load , 2004, Nature Neuroscience.

[28]  D. Tank,et al.  Persistent neural activity: prevalence and mechanisms , 2004, Current Opinion in Neurobiology.

[29]  C. Koch,et al.  Brain Areas Specific for Attentional Load in a Motion-Tracking Task , 2001, Journal of Cognitive Neuroscience.

[30]  J. Duncan Selective attention and the organization of visual information. , 1984, Journal of experimental psychology. General.

[31]  Leila Reddy,et al.  Top–down biases win against focal attention in the fusiform face area , 2007, NeuroImage.

[32]  H. Pashler The Psychology of Attention , 1997 .

[33]  Nilli Lavie,et al.  The role of perceptual load in visual awareness , 2006, Brain Research.

[34]  M. Corbetta,et al.  Areas Involved in Encoding and Applying Directional Expectations to Moving Objects , 1999, The Journal of Neuroscience.

[35]  Geraint Rees,et al.  Top–Down Modulation of Human Early Visual Cortex after Stimulus Offset Supports Successful Postcued Report , 2011, Journal of Cognitive Neuroscience.

[36]  R. Dolan,et al.  Attentional load and sensory competition in human vision: modulation of fMRI responses by load at fixation during task-irrelevant stimulation in the peripheral visual field. , 2005, Cerebral cortex.

[37]  J. V. von Wright,et al.  Selection in Visual Immediate Memory , 1968, Acta psychologica.

[38]  B. Julesz,et al.  Withdrawing attention at little or no cost: Detection and discrimination tasks , 1998, Perception & psychophysics.

[39]  George Sperling,et al.  The information available in brief visual presentations. , 1960 .

[40]  J. Braun Vision and attention: the role of training , 1998, Nature.

[41]  N. Kanwisher,et al.  Visual attention: Insights from brain imaging , 2000, Nature Reviews Neuroscience.

[42]  B. Dow,et al.  Orientation and color columns in monkey visual cortex. , 2002, Cerebral cortex.