Specific and Nonspecific Neural Activity during Selective Processing of Visual Representations in Working Memory

In this fMRI study, we investigated prefrontal cortex (PFC) and visual association regions during selective information processing. We recorded behavioral responses and neural activity during a delayed recognition task with a cue presented during the delay period. A specific cue (“Face” or “Scene”) was used to indicate which one of the two initially viewed pictures of a face and a scene would be tested at the end of a trial, whereas a nonspecific cue (“Both”) was used as control. As expected, the specific cues facilitated behavioral performance (faster response times) compared to the nonspecific cue. A postexperiment memory test showed that the items cued to remember were better recognized than those not cued. The fMRI results showed largely overlapped activations across the three cue conditions in dorsolateral and ventrolateral PFC, dorsomedial PFC, posterior parietal cortex, ventral occipito-temporal cortex, dorsal striatum, and pulvinar nucleus. Among those regions, dorsomedial PFC and inferior occipital gyrus remained active during the entire postcue delay period. Differential activity was mainly found in the association cortices. In particular, the parahippocampal area and posterior superior parietal lobe showed significantly enhanced activity during the postcue period of the scene condition relative to the Face and Both conditions. No regions showed differentially greater responses to the face cue. Our findings suggest that a better representation of visual information in working memory may depend on enhancing the more specialized visual association areas or their interaction with PFC.

[1]  Michael D. Dodd,et al.  In Opposition to Inhibition , 2003 .

[2]  O. Hikosaka,et al.  What and When: Parallel and Convergent Processing in Motor Control , 2000, The Journal of Neuroscience.

[3]  Colin M. Macleod,et al.  Direct versus indirect tests of memory: Directed forgetting meets the generation effect , 2000, Psychonomic bulletin & review.

[4]  T. Allison,et al.  Face-sensitive regions in human extrastriate cortex studied by functional MRI. , 1995, Journal of neurophysiology.

[5]  G. Holmes The prefrontal cortex: Anatomy, physiology, and neuropsychology of the frontal lobe (2nd ed.) , 1989 .

[6]  Leslie G. Ungerleider,et al.  Transient and sustained activity in a distributed neural system for human working memory , 1997, Nature.

[7]  Hoi-Chung Leung,et al.  Load response functions in the human spatial working memory circuit during location memory updating , 2007, NeuroImage.

[8]  N. Kanwisher Domain specificity in face perception , 2000, Nature Neuroscience.

[9]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[10]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[11]  Adam Gazzaley,et al.  Functional interactions between prefrontal and visual association cortex contribute to top-down modulation of visual processing. , 2007, Cerebral cortex.

[12]  T. Egner,et al.  Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information , 2005, Nature Neuroscience.

[13]  P. Goldman-Rakic Circuitry of Primate Prefrontal Cortex and Regulation of Behavior by Representational Memory , 2011 .

[14]  Adam Gazzaley,et al.  Measuring functional connectivity during distinct stages of a cognitive task , 2004, NeuroImage.

[15]  M. Shen,et al.  Contralateral delay activity tracks object identity information in visual short term memory , 2011, Brain Research.

[16]  David Friedman,et al.  Event-related potential (ERP) measures reveal the timing of memory selection processes and proactive interference resolution in working memory , 2011, Brain Research.

[17]  M. D’Esposito,et al.  Dissecting Contributions of Prefrontal Cortex and Fusiform Face Area to Face Working Memory , 2003, Journal of Cognitive Neuroscience.

[18]  Colin M. Macleod Directed forgetting affects both direct and indirect tests of memory. , 1989 .

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

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

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

[22]  Hoi-Chung Leung,et al.  Linear and nonlinear prefrontal and parietal activity during multiple-item working memory , 2011, NeuroImage.

[23]  M. D’Esposito,et al.  An Area within Human Ventral Cortex Sensitive to “Building” Stimuli Evidence and Implications , 1998, Neuron.

[24]  William Hirst,et al.  MEM: Memory Subsystems as Processes , 2019, Theories of Memory.

[25]  Hoi-Chung Leung,et al.  Interference resolution in spatial working memory , 2004, NeuroImage.

[26]  N. Cowan An embedded-processes model of working memory , 1999 .

[27]  Marcia K. Johnson,et al.  A brief thought can modulate activity in extrastriate visual areas: Top-down effects of refreshing just-seen visual stimuli , 2007, NeuroImage.

[28]  Hoi-Chung Leung,et al.  Frontal activations associated with accessing and evaluating information in working memory: an fMRI study , 2003, NeuroImage.

[29]  E E Smith,et al.  The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[30]  G. F. Tremblay,et al.  The Prefrontal Cortex , 1989, Neurology.

[31]  William A. Cunningham,et al.  Using fMRI to investigate a component process of reflection: Prefrontal correlates of refreshing a just-activated representation , 2016 .

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

[33]  S. Thompson-Schill Neuroimaging studies of semantic memory: inferring “how” from “where” , 2003, Neuropsychologia.

[34]  Edward E. Smith,et al.  Neuroimaging studies of working memory: , 2003, Cognitive, affective & behavioral neuroscience.

[35]  Marcia K. Johnson MEM: Mechanisms of Recollection , 1992, Journal of Cognitive Neuroscience.

[36]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[37]  Y. Miyashita,et al.  Top-down signal from prefrontal cortex in executive control of memory retrieval , 1999, Nature.

[38]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[39]  S. Yantis,et al.  Cortical mechanisms of space-based and object-based attentional control , 2003, Current Opinion in Neurobiology.

[40]  A. Ishai,et al.  Distributed neural systems for the generation of visual images , 2000, NeuroImage.

[41]  G. Humphreys,et al.  The role of the pulvinar in resolving competition between memory and visual selection: A functional connectivity study , 2011, Neuropsychologia.

[42]  Marcia K. Johnson,et al.  Refreshing: A Minimal Executive Function , 2007, Cortex.

[43]  John Brown The Nature of Set-to-Learn and of Intra-Material Interference in Immediate Memory , 1954 .

[44]  Leslie G. Ungerleider,et al.  Distributed Neural Systems for the Generation of Visual Images , 2000, Neuron.

[45]  John Jonides,et al.  Dissociable neural mechanisms underlying response-based and familiarity-based conflict in working memory , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[46]  J. Jonides,et al.  Inhibition in verbal working memory revealed by brain activation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Robert A. Bjork,et al.  Varieties of goal-directed forgetting , 1998 .

[48]  M. D’Esposito Working memory. , 2008, Handbook of clinical neurology.

[49]  M. J. Emerson,et al.  The Unity and Diversity of Executive Functions and Their Contributions to Complex “Frontal Lobe” Tasks: A Latent Variable Analysis , 2000, Cognitive Psychology.

[50]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[51]  M. D’Esposito,et al.  Functional connectivity during working memory maintenance , 2004, Cognitive, affective & behavioral neuroscience.

[52]  Jens Schwarzbach,et al.  Control of object-based attention in human cortex. , 2004, Cerebral cortex.

[53]  Marcia K. Johnson,et al.  Refreshing One of Several Active Representations: Behavioral and Functional Magnetic Resonance Imaging Differences between Young and Older Adults , 2008, Journal of Cognitive Neuroscience.

[54]  Lila Davachi,et al.  When Keeping in Mind Supports Later Bringing to Mind: Neural Markers of Phonological Rehearsal Predict Subsequent Remembering , 2001, Journal of Cognitive Neuroscience.

[55]  B. Postle,et al.  Using event-related fMRI to assess delay-period activity during performance of spatial and nonspatial working memory tasks. , 2000, Brain research. Brain research protocols.

[56]  D. V. von Cramon,et al.  Functional organization of the lateral premotor cortex: fMRI reveals different regions activated by anticipation of object properties, location and speed. , 2001, Brain research. Cognitive brain research.

[57]  M D'Esposito,et al.  The roles of prefrontal brain regions in components of working memory: effects of memory load and individual differences. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[58]  K. Oberauer Access to information in working memory: exploring the focus of attention. , 2002, Journal of experimental psychology. Learning, memory, and cognition.

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

[60]  J. Tanji Sequential organization of multiple movements: involvement of cortical motor areas. , 2001, Annual review of neuroscience.

[61]  N. Cowan Attention and Memory: An Integrated Framework , 1995 .

[62]  Hoi-Chung Leung,et al.  The effect of memory load on cortical activity in the spatial working memory circuit , 2004, Cognitive, affective & behavioral neuroscience.

[63]  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.

[64]  E. Koechlin,et al.  The role of the anterior prefrontal cortex in human cognition , 1999, Nature.

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

[66]  J. Fuster The Prefrontal Cortex , 1997 .

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