Selective Attention Supports Working Memory Maintenance by Modulating Perceptual Processing of Distractors

Selective attention has been shown to bias sensory processing in favor of relevant stimuli and against irrelevant or distracting stimuli in perceptual tasks. Increasing evidence suggests that selective attention plays an important role during working memory maintenance, possibly by biasing sensory processing in favor of to-be-remembered items. In the current study, we investigated whether selective attention may also support working memory by biasing processing against irrelevant and potentially distracting information. Event-related potentials (ERPs) were recorded while subjects (n 22) performed a delayed-recognition task for faces and shoes. The delay period was filled with face or shoe distractors. Behavioral performance was impaired when distractors were congruent with the working memory domain (e.g., face distractor during working memory for faces) relative to when distractors were incongruent with the working memory domain (e.g., face distractor during shoe working memory). If attentional biasing against distractor processing is indeed functionally relevant in supporting working memory maintenance, perceptual processing of distractors is predicted to be attenuated when distractors are more behaviorally intrusive relative to when they are nonintrusive. As such, we predicted that perceptual processing of distracting faces, as measured by the face-sensitive N170 ERP component, would be reduced in the context of congruent (face) working memory relative to incongruent (shoe) working memory. The N170 elicited by distracting faces demonstrated reduced amplitude during congruent versus incongruent working memory. These results suggest that perceptual processing of distracting faces may be attenuated due to attentional biasing against sensory processing of distractors that are most behaviorally intrusive during working memory maintenance.

[1]  C. Frith,et al.  The Role of Working Memory in Visual Selective Attention , 2001, Science.

[2]  A. Jha,et al.  Tracking the time-course of attentional involvement in spatial working memory: an event-related potential investigation. , 2002, Brain research. Cognitive brain research.

[3]  E. Viding,et al.  Load theory of selective attention and cognitive control. , 2004, Journal of experimental psychology. General.

[4]  G. McCarthy,et al.  The Influence of Memory Load Upon Delay-Interval Activity in a Working-Memory Task: An Event-Related Functional MRI Study , 2000, Journal of Cognitive Neuroscience.

[5]  J. Tanaka,et al.  A Neural Basis for Expert Object Recognition , 2001, Psychological science.

[6]  R. Passingham,et al.  Active maintenance in prefrontal area 46 creates distractor-resistant memory , 2002, Nature Neuroscience.

[7]  N. Lavie,et al.  On the Efficiency of Visual Selective Attention: Efficient Visual Search Leads to Inefficient Distractor Rejection , 1997 .

[8]  S. Hillyard,et al.  Event-related brain potentials in the study of visual selective attention. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[9]  N. Lavie Perceptual load as a necessary condition for selective attention. , 1995, Journal of experimental psychology. Human perception and performance.

[10]  Margot J. Taylor,et al.  Source analysis of the N170 to faces and objects , 2004, Neuroreport.

[11]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

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

[13]  C. Joyce,et al.  The face-sensitive N170 and VPP components manifest the same brain processes: The effect of reference electrode site , 2005, Clinical Neurophysiology.

[14]  H. Bülthoff,et al.  Face recognition under varying poses: The role of texture and shape , 1996, Vision Research.

[15]  M. Tarr,et al.  The N170 occipito‐temporal component is delayed and enhanced to inverted faces but not to inverted objects: an electrophysiological account of face‐specific processes in the human brain , 2000, Neuroreport.

[16]  Margot J. Taylor,et al.  Is the face‐sensitive N170 the only ERP not affected by selective attention? , 2000, Neuroreport.

[17]  M. Tarr,et al.  Expertise Training with Novel Objects Leads to Left-Lateralized Facelike Electrophysiological Responses , 2002, Psychological science.

[18]  N. Lavie,et al.  The Role of Perceptual Load in Processing Distractor Faces , 2003, Psychological science.

[19]  M. Eimer Effects of face inversion on the structural encoding and recognition of faces. Evidence from event-related brain potentials. , 2000, Brain research. Cognitive brain research.

[20]  Maro G. Machizawa,et al.  Neural measures reveal individual differences in controlling access to working memory , 2005, Nature.

[21]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[22]  Kartik K. Sreenivasan,et al.  Temporal Characteristics of Top-Down Modulations during Working Memory Maintenance: An Event-related Potential Study of the N170 Component , 2007, Journal of Cognitive Neuroscience.

[23]  Robert T. Knight,et al.  Top-down Enhancement and Suppression of the Magnitude and Speed of Neural Activity , 2005, Journal of Cognitive Neuroscience.

[24]  M. Tarr,et al.  Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects , 1999, Nature Neuroscience.

[25]  T. Allison,et al.  Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. , 1999, Cerebral cortex.

[26]  Charles T. Leonard,et al.  The effect of intervening forces on finger force perception , 2008, Neuroscience Letters.

[27]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[28]  M. Tarr,et al.  Visual expertise with nonface objects leads to competition with the early perceptual processing of faces in the human occipitotemporal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Eimer,et al.  The processing of emotional facial expression is gated by spatial attention: evidence from event-related brain potentials. , 2003, Brain research. Cognitive brain research.

[30]  Margot J. Taylor,et al.  N170 or N1? Spatiotemporal differences between object and face processing using ERPs. , 2004, Cerebral cortex.

[31]  I. Gauthier,et al.  Perceptual interference supports a non-modular account of face processing , 2003, Nature Neuroscience.

[32]  D. Woods,et al.  The habituation of event-related potentials to speech sounds and tones. , 1986, Electroencephalography and clinical neurophysiology.

[33]  Edward E. Smith,et al.  Rehearsal in Spatial Working Memory: Evidence From Neuroimaging , 1999 .

[34]  M. Eimer ATTENTIONAL MODULATIONS OF EVENT-RELATED BRAIN POTENTIALS SENSITIVE TO FACES , 2000, Cognitive neuropsychology.

[35]  E. Vogel,et al.  Interactions between attention and working memory , 2006, Neuroscience.

[36]  T. Allison,et al.  Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. , 1999, Cerebral cortex.

[37]  H. Semlitsch,et al.  A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. , 1986, Psychophysiology.

[38]  R. Knight,et al.  Contribution of Human Prefrontal Cortex to Delay Performance , 1998, Journal of Cognitive Neuroscience.

[39]  Amishi P. Jha,et al.  The role of prefrontal cortex in resolving distractor interference , 2004, Cognitive, affective & behavioral neuroscience.

[40]  Bradley R. Postle,et al.  Delay-period Activity in the Prefrontal Cortex: One Function Is Sensory Gating , 2005, Journal of Cognitive Neuroscience.

[41]  E. Vogel,et al.  Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[42]  N. Lavie Distracted and confused?: Selective attention under load , 2005, Trends in Cognitive Sciences.

[43]  Roxane J. Itier,et al.  Face, eye and object early processing: What is the face specificity? , 2006, NeuroImage.