Working memory of somatosensory stimuli: an fMRI study.

In a previous study, we have shown that passive recognition of tactile geometrical shapes (i.e. no exploratory movement) engages prefrontal and premotor areas in addition to somatosensory regions (Savini et al., 2010). In the present study we tested the hypothesis that these regions are involved not only in the perception but also during working memory of such somatic information. We performed functional magnetic resonance imaging (fMRI) during the execution of N-BACK tasks, with 2D geometrical shapes blindly pressed on the subjects' right hand palm. Three conditions with increasing memory load (0-BACK, 1-BACK, 2-BACK) were used. Results showed that primary somatosensory area (SI), secondary somatosensory area (SII) and bilateral Insula were active in all conditions, confirming their importance in coding somatosensory stimuli. Activation of fronto-parietal circuit in supplementary motor area (SMA), right superior parietal lobe (rSPL), bilateral middle frontal gyrus, left inferior frontal gyrus, and right superior frontal sulcus was significantly larger during 1-BACK and 2-BACK than 0-BACK. Left superior parietal lobe and right frontal eye field showed a higher activation during the 2-BACK than 0-BACK. Finally, SMA and rSPL were characterized by a statistically significant higher activation during 2-BACK than 1-BACK, revealing their sensitivity to the memory load. These results suggest that working memory of tactile geometrical shapes (no exploratory movement) involves a complex circuit of modal and supramodal fronto-parietal areas.

[1]  P. Rossini,et al.  Passive tactile recognition of geometrical shape in humans: An fMRI study , 2010, Brain Research Bulletin.

[2]  Margaret E. Sereno,et al.  Shape selectivity in primate frontal eye field. , 2008, Journal of neurophysiology.

[3]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

[4]  H Burton,et al.  Ipsilateral intracortical connections of physiologically defined cutaneous representations in areas 3b and 1 of macaque monkeys: Projections in the vicinity of the central sulcus , 1995, The Journal of comparative neurology.

[5]  Edward E. Smith,et al.  The Role of Parietal Cortex in Verbal Working Memory , 1998, The Journal of Neuroscience.

[6]  P. Goldman-Rakic Regional and cellular fractionation of working memory. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[8]  Hannu J. Aronen,et al.  Working Memory of Identification of Emotional Vocal Expressions: An fMRI Study , 2001, NeuroImage.

[9]  S. Petersen,et al.  Influences of lesions of parietal cortex on visual spatial attention in humans , 2004, Experimental Brain Research.

[10]  P. Roland,et al.  Supplementary motor area and other cortical areas in organization of voluntary movements in man. , 1980, Journal of neurophysiology.

[11]  Takashi R Sato,et al.  Neuronal Basis of Covert Spatial Attention in the Frontal Eye Field , 2005, The Journal of Neuroscience.

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

[13]  S. Carlson,et al.  Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. , 1998, Cerebral cortex.

[14]  J. Tanji,et al.  A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task. , 1992, Journal of neurophysiology.

[15]  M. Guazzelli,et al.  Tactile spatial working memory activates the dorsal extrastriate cortical pathway in congenitally blind individuals. , 2008, Archives italiennes de biologie.

[16]  Edward E. Smith,et al.  Dissociation of Storage and Rehearsal in Verbal Working Memory: Evidence From Positron Emission Tomography , 1996 .

[17]  C. Cassanello,et al.  Frontal Eye Field Neurons Signal Changes in Decision Criteria , 2009, Nature Neuroscience.

[18]  A. Baddeley Working memory: looking back and looking forward , 2003, Nature Reviews Neuroscience.

[19]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[20]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[21]  C. Bruce,et al.  Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. , 1985, Journal of neurophysiology.

[22]  Emiliano Ricciardi,et al.  Beyond sensory images: Object-based representation in the human ventral pathway. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[23]  V. Ferrera,et al.  Radial motion bias in macaque frontal eye field , 2006, Visual Neuroscience.

[24]  A Baddeley,et al.  The fractionation of working memory. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. Tsakiris My body in the brain: A neurocognitive model of body-ownership , 2010, Neuropsychologia.

[26]  J. Hajnal,et al.  Artifacts due to stimulus correlated motion in functional imaging of the brain , 1994, Magnetic resonance in medicine.

[27]  Henrik Walter,et al.  Evidence for Quantitative Domain Dominance for Verbal and Spatial Working Memory in Frontal and Parietal Cortex , 2003, Cortex.

[28]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[29]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[30]  Karl J. Friston,et al.  Distribution of cortical neural networks involved in word comprehension and word retrieval. , 1991, Brain : a journal of neurology.

[31]  E. Rolls The affective and cognitive processing of touch, oral texture, and temperature in the brain , 2010, Neuroscience & Biobehavioral Reviews.

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

[33]  Edward E. Smith,et al.  PET Evidence for an Amodal Verbal Working Memory System , 1996, NeuroImage.

[34]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[35]  J. Jonides,et al.  Neuroimaging analyses of human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[37]  D. Ferrier The Functions of the Brain , 1887, Edinburgh Medical Journal.

[38]  E. Bullmore,et al.  Statistical methods of estimation and inference for functional MR image analysis , 1996, Magnetic resonance in medicine.

[39]  P. Pietrini,et al.  Neural correlates of spatial working memory in humans: A functional magnetic resonance imaging study comparing visual and tactile processes , 2006, Neuroscience.

[40]  Serge A R B Rombouts,et al.  Functional brain connectivity at rest changes after working memory training , 2013, Human brain mapping.

[41]  Claudio Babiloni,et al.  Functional topography of the secondary somatosensory cortex for nonpainful and painful stimulation of median and tibial nerve: an fMRI study , 2004, NeuroImage.

[42]  S Martinkauppi,et al.  Working memory of auditory localization. , 2000, Cerebral cortex.

[43]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[44]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[45]  Edward E. Smith,et al.  A Parametric Study of Prefrontal Cortex Involvement in Human Working Memory , 1996, NeuroImage.

[46]  J. Jonides,et al.  Overlapping mechanisms of attention and spatial working memory , 2001, Trends in Cognitive Sciences.

[47]  Edward E. Smith,et al.  Working Memory: A View from Neuroimaging , 1997, Cognitive Psychology.

[48]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[49]  A. Haley,et al.  Functional imaging of working memory and peripheral endothelial function in middle-aged adults , 2010, Brain and Cognition.

[50]  Rüdiger J. Seitz,et al.  A fronto-parietal circuit for tactile object discrimination: an event-related fMRI study , 2003, NeuroImage.

[51]  J. Schall,et al.  Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  Katherine M. Armstrong,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2003, Nature.

[53]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[54]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[55]  Robin M. Chan,et al.  Working memory for complex figures: an fMRI comparison of letter and fractal n-back tasks. , 2002, Neuropsychology.