Maintenance and manipulation of somatosensory information in ventrolateral prefrontal cortex

Neuroimaging studies of working memory (WM) suggest that prefrontal cortex may assist sustained maintenance, but also internal manipulation, of stimulus representations in lower‐level areas. A different line of research in the somatosensory domain indicates that neuronal activity in ventrolateral prefrontal cortex (VLPFC) may also represent specific memory contents in itself, however leaving open to what extent top‐down control on lower‐level areas is exerted, or how internal manipulation processes are implemented. We used functional imaging and connectivity analysis to study static maintenance and internal manipulation of tactile working memory contents after physically identical stimulation conditions, in human subjects. While both tasks recruited similar subareas in the inferior frontal gyrus (IFG) in VLPFC, static maintenance of the tactile information was additionally characterized by increased functional coupling between IFG and primary somatosensory cortex. Independently, during internal manipulation, a quantitative representation of the task‐relevant information was evident in IFG itself, even in the absence of physical stimulation. Together, these findings demonstrate the functional diversity of activity within VLPFC according to different working memory demands, and underline the role of IFG as a core region in sensory WM processing. Hum Brain Mapp 35:2412–2423, 2014. © 2013 Wiley Periodicals, Inc.

[1]  Felix Blankenburg,et al.  Supramodal Parametric Working Memory Processing in Humans , 2012, The Journal of Neuroscience.

[2]  A. Kleinschmidt,et al.  Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Karl J. Friston,et al.  Neural Coding of Tactile Decisions in the Human Prefrontal Cortex , 2006, The Journal of Neuroscience.

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

[5]  S. Courtney,et al.  Attention and cognitive control as emergent properties of information representation in working memory , 2004, Cognitive, affective & behavioral neuroscience.

[6]  Theodore P. Zanto,et al.  Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory , 2011, Nature Neuroscience.

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

[8]  Felix Blankenburg,et al.  Stimulus-dependent EEG activity reflects internal updating of tactile working memory in humans , 2011, Proceedings of the National Academy of Sciences.

[9]  Felix Blankenburg,et al.  Oscillatory Correlates of Vibrotactile Frequency Processing in Human Working Memory , 2010, The Journal of Neuroscience.

[10]  Mark D'Esposito,et al.  Searching for “the Top” in Top-Down Control , 2005, Neuron.

[11]  N. Logothetis,et al.  Frequency-Band Coupling in Surface EEG Reflects Spiking Activity in Monkey Visual Cortex , 2009, Neuron.

[12]  K. Bäuml,et al.  The Relationship between Brain Oscillations and BOLD Signal during Memory Formation: A Combined EEG–fMRI Study , 2011, The Journal of Neuroscience.

[13]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[14]  R. Goebel,et al.  Content- and Task-Specific Dissociations of Frontal Activity during Maintenance and Manipulation in Visual Working Memory , 2006, The Journal of Neuroscience.

[15]  Mark D'Esposito,et al.  From cognitive to neural models of working memory , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[17]  Felix Blankenburg,et al.  Working memory coding of analog stimulus properties in the human prefrontal cortex. , 2014, Cerebral cortex.

[18]  Raymond J Dolan,et al.  Maintenance versus manipulation in verbal working memory revisited: an fMRI study , 2003, NeuroImage.

[19]  Bart Aben,et al.  About the Distinction between Working Memory and Short-Term Memory , 2012, Front. Psychology.

[20]  C. Fiebach,et al.  Modulation of Inferotemporal Cortex Activation during Verbal Working Memory Maintenance , 2006, Neuron.

[21]  Felix Blankenburg,et al.  Impairing somatosensory working memory using rTMS , 2011, The European journal of neuroscience.

[22]  J. Driver,et al.  Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[23]  Joshua W. Brown,et al.  A meta-analysis of executive components of working memory. , 2013, Cerebral cortex.

[24]  Michael Petrides,et al.  Ventrolateral prefrontal cortex and tactile memory disambiguation in the human brain , 2007, Proceedings of the National Academy of Sciences.

[25]  Felix Blankenburg,et al.  Tactile Motion and Pattern Processing Assessed with High-Field fMRI , 2011, PloS one.

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

[27]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[28]  Jochen Kaiser,et al.  Basic operations in working memory: Contributions from functional imaging studies , 2010, Behavioural Brain Research.

[29]  J. Serences,et al.  Neural system for controlling the contents of object working memory in humans. , 2006, Cerebral cortex.

[30]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[31]  Rainer Goebel,et al.  The neural substrate for working memory of tactile surface texture , 2013, Human brain mapping.

[32]  Clayton E. Curtis,et al.  Differential effects of distraction during working memory on delay-period activity in the prefrontal cortex and the visual association cortex , 2006, NeuroImage.

[33]  Tyrone D. Cannon,et al.  Maintenance and Manipulation in Spatial Working Memory: Dissociations in the Prefrontal Cortex , 2002, NeuroImage.

[34]  P. Goldman-Rakic Cellular basis of working memory , 1995, Neuron.

[35]  P. Goldman-Rakic,et al.  Segregation of working memory functions within the dorsolateral prefrontal cortex , 2000, Experimental Brain Research.

[36]  Rainer Goebel,et al.  The neural correlates of human working memory for haptically explored object orientations. , 2007, Cerebral cortex.

[37]  Arno Villringer,et al.  Neural Correlates of Vibrotactile Working Memory in the Human Brain , 2006, The Journal of Neuroscience.

[38]  Katja Fiehler,et al.  Working memory maintenance of grasp-target information in the human posterior parietal cortex , 2011, NeuroImage.

[39]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[40]  Alan C. Evans,et al.  Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[41]  A. Baddeley Human Memory: Theory and Practice, Revised Edition , 1990 .

[42]  Geraint Rees,et al.  The Cutaneous Rabbit Illusion Affects Human Primary Sensory Cortex Somatotopically , 2006, PLoS biology.

[43]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[44]  Rupert Lanzenberger,et al.  Correlations and anticorrelations in resting-state functional connectivity MRI: A quantitative comparison of preprocessing strategies , 2009, NeuroImage.

[45]  A. Nobre,et al.  Top-down modulation: bridging selective attention and working memory , 2012, Trends in Cognitive Sciences.