Visual Short-term Memory Load Reduces Retinotopic Cortex Response to Contrast

Load Theory of attention suggests that high perceptual load in a task leads to reduced sensory visual cortex response to task-unrelated stimuli resulting in “load-induced blindness” [e.g., Lavie, N. Attention, distraction and cognitive control under load. Current Directions in Psychological Science, 19, 143–148, 2010; Lavie, N. Distracted and confused?: Selective attention under load. Trends in Cognitive Sciences, 9, 75–82, 2005]. Consideration of the findings that visual STM (VSTM) involves sensory recruitment [e.g., Pasternak, T., & Greenlee, M. Working memory in primate sensory systems. Nature Reviews Neuroscience, 6, 97–107, 2005] within Load Theory led us to a new hypothesis regarding the effects of VSTM load on visual processing. If VSTM load draws on sensory visual capacity, then similar to perceptual load, high VSTM load should also reduce visual cortex response to incoming stimuli leading to a failure to detect them. We tested this hypothesis with fMRI and behavioral measures of visual detection sensitivity. Participants detected the presence of a contrast increment during the maintenance delay in a VSTM task requiring maintenance of color and position. Increased VSTM load (manipulated by increased set size) led to reduced retinotopic visual cortex (V1–V3) responses to contrast as well as reduced detection sensitivity, as we predicted. Additional visual detection experiments established a clear tradeoff between the amount of information maintained in VSTM and detection sensitivity, while ruling out alternative accounts for the effects of VSTM load in terms of differential spatial allocation strategies or task difficulty. These findings extend Load Theory to demonstrate a new form of competitive interactions between early visual cortex processing and visual representations held in memory under load and provide a novel line of support for the sensory recruitment hypothesis of VSTM.

[1]  Edward F. Ester,et al.  PSYCHOLOGICAL SCIENCE Research Article Stimulus-Specific Delay Activity in Human Primary Visual Cortex , 2022 .

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

[3]  H. Kesten Accelerated Stochastic Approximation , 1958 .

[4]  Ana Torralbo,et al.  Perceptual-Load-Induced Selection as a Result of Local Competitive Interactions in Visual Cortex , 2008, Psychological science.

[5]  Jan Theeuwes,et al.  Spatial working memory effects in early visual cortex , 2010, Brain and Cognition.

[6]  Daniel J. Mitchell,et al.  Flexible, capacity-limited activity of posterior parietal cortex in perceptual as well as visual short-term memory tasks. , 2008, Cerebral cortex.

[7]  Leslie G. Ungerleider,et al.  Neural Correlates of Visual Working Memory fMRI Amplitude Predicts Task Performance , 2002, Neuron.

[8]  B. Postle Working memory as an emergent property of the mind and brain , 2006, Neuroscience.

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

[10]  Zachary J. J. Roper,et al.  Visual short-term memory load strengthens selective attention , 2014, Psychonomic bulletin & review.

[11]  Andrew R. A. Conway,et al.  On the capacity of attention: Its estimation and its role in working memory and cognitive aptitudes , 2005, Cognitive Psychology.

[12]  Edward F. Ester,et al.  Spatially Global Representations in Human Primary Visual Cortex during Working Memory Maintenance , 2009, The Journal of Neuroscience.

[13]  H Spekreijse,et al.  A Neural Correlate of Working Memory in the Monkey Primary Visual Cortex , 2001, Science.

[14]  Maki S. Koyama,et al.  Cerebral mechanisms for different second language writing systems , 2013, Neuropsychologia.

[15]  G. V. Simpson,et al.  Phase Locking of Single Neuron Activity to Theta Oscillations during Working Memory in Monkey Extrastriate Visual Cortex , 2003, Neuron.

[16]  James W Bisley,et al.  Activity of neurons in cortical area MT during a memory for motion task. , 2004, Journal of neurophysiology.

[17]  T. Pasternak,et al.  Working memory in primate sensory systems , 2005, Nature Reviews Neuroscience.

[18]  R. Conrad,et al.  Acoustic confusions in immediate memory. , 1964 .

[19]  Nikos Konstantinou,et al.  The role of visual short term memory load in visual sensory detection , 2011 .

[20]  N. Lavie Attention, Distraction, and Cognitive Control Under Load , 2010 .

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

[22]  B. Postle,et al.  Maintenance versus Manipulation of Information Held in Working Memory: An Event-Related fMRI Study , 1999, Brain and Cognition.

[23]  B. Wandell,et al.  Visualization and Measurement of the Cortical Surface , 2000, Journal of Cognitive Neuroscience.

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

[25]  F. Tong,et al.  Decoding reveals the contents of visual working memory in early visual areas , 2009, Nature.

[26]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

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

[28]  Kartik K. Sreenivasan,et al.  Selective Attention Supports Working Memory Maintenance by Modulating Perceptual Processing of Distractors , 2007, Journal of Cognitive Neuroscience.

[29]  Nilli Lavie,et al.  Load Induced Blindness , 2008, Journal of experimental psychology. Human perception and performance.

[30]  C. Marshuetz,et al.  Order information in working memory: an integrative review of evidence from brain and behavior. , 2005, Psychological bulletin.

[31]  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.

[32]  Juha Silvanto,et al.  How visual short-term memory maintenance modulates the encoding of external input: Evidence from concurrent visual adaptation and TMS , 2013, NeuroImage.

[33]  Nilli Lavie,et al.  Neural generators of sustained activity differ for stimulus‐encoding and delay maintenance , 2009, The European journal of neuroscience.

[34]  Christian Büchel,et al.  The functional and temporal characteristics of top-down modulation in visual selection. , 2005, Cerebral cortex.

[35]  Igor Schindler,et al.  An exploration of the role of the superior temporal gyrus in visual search and spatial perception using TMS , 2014 .

[36]  S. Ferber,et al.  Spatial awareness is a function of the temporal not the posterior parietal lobe , 2001, Nature.

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

[38]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[39]  M. D’Esposito,et al.  The effect of non-visual working memory load on top-down modulation of visual processing , 2009, Neuropsychologia.

[40]  E. Vogel,et al.  Capacity limit of visual short-term memory in human posterior parietal cortex , 2004 .

[41]  N. Lavie,et al.  The role of working memory in attentional capture , 2005, Psychonomic bulletin & review.

[42]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

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

[44]  T. A. Kelley,et al.  Working Memory Load Modulates Distractor Competition in Primary Visual Cortex , 2010, Cerebral cortex.

[45]  M. Chun,et al.  Dissociable neural mechanisms supporting visual short-term memory for objects , 2006, Nature.