Task-Relevant Modulation of Contralateral and Ipsilateral Primary Somatosensory Cortex and the Role of a Prefrontal-Cortical Sensory Gating System

Electrophysiological studies have shown that task-relevant somatosensory information leads to selective facilitation within the primary somatosensory cortex (SI). The purpose of the present study was (1) to further explore the relationship between the relevancy of stimuli and activation within the contralateral and ipsilateral SI and (2) to provide further insight into the specific sensory gating network responsible for modulating neural activity within SI. Functional MRI of 12 normal subjects was performed with vibrotactile stimuli presented to the pad of the index finger. In experiment 1, the stimulus was presented to either the left or the right hand. Subjects were required to detect transient changes in stimulus frequency. In experiment 2, stimuli were presented to either the right hand alone or both hands simultaneously. Stimuli were applied either (A) passively or (B) when subjects were asked to detect frequency changes that occurred to the right hand only. In experiment 1, task-relevant somatosensory stimulation led not only to enhanced contralateral SI activity, but also to a suppression of activity in the ipsilateral SI. In experiment 2, SI activation was enhanced when stimuli were task-relevant, compared to that observed with passive input. When stimuli were presented simultaneously to both hands, only those that were task-relevant increased SI activation. This was associated with recruitment of a network of cortical regions, including the right prefrontal cortex (Brodmann area 9). We conclude that SI modulation is dependent on task relevancy and that this modulation may be regulated, at least in part, by the prefrontal cortex.

[1]  F. N. Dempster,et al.  Interference and inhibition in cognition: An historical perspective , 1995 .

[2]  Tetsuro Yamamoto,et al.  Short latency activation of local circuit neurons in the cat somatosensory cortex , 1988, Brain Research.

[3]  J. Misiaszek,et al.  Movement-induced gain modulation of somatosensory potentials and soleus H-reflexes evoked from the leg I. Kinaesthetic task demands , 1997, Experimental Brain Research.

[4]  E C Wong,et al.  Processing strategies for time‐course data sets in functional mri of the human brain , 1993, Magnetic resonance in medicine.

[5]  W. McIlroy,et al.  Task‐relevant selective modulation of somatosensory afferent paths from the lower limb , 2000, Neuroreport.

[6]  M. E. Raichle,et al.  PET Studies of Auditory and Phonological Processing: Effects of Stimulus Characteristics and Task Demands , 1995, Journal of Cognitive Neuroscience.

[7]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  Robert T. Knight,et al.  Prefrontal cortex gating of auditory transmission in humans , 1989, Brain Research.

[9]  R. Knight,et al.  Prefrontal cortex regulates inhibition and excitation in distributed neural networks. , 1999, Acta psychologica.

[10]  M. Corbetta,et al.  Top-down modulation of early sensory cortex. , 1997 .

[11]  R. Knight,et al.  Gating of somatosensory input by human prefrontal cortex , 1990, Brain Research.

[12]  D. Pandya,et al.  Architecture and Connections of the Frontal Lobe , 2019, The Frontal Lobes Revisited.

[13]  S. Knecht,et al.  Facilitation of somatosensory evoked potentials by exploratory finger movements , 2004, Experimental Brain Research.

[14]  R. Guillery,et al.  Paying attention to the thalamic reticular nucleus , 1998, Trends in Neurosciences.

[15]  G. Glover,et al.  Self‐navigated spiral fMRI: Interleaved versus single‐shot , 1998, Magnetic resonance in medicine.

[16]  S. Stone-Elander,et al.  Coexistence of Attention-Based Facilitation and Inhibition in the Human Cortex , 1998, NeuroImage.

[17]  W. Neill,et al.  Selective attention and the inhibitory control of cognition. , 1995 .

[18]  C E Chapman,et al.  Active versus passive touch: factors influencing the transmission of somatosensory signals to primary somatosensory cortex. , 1994, Canadian journal of physiology and pharmacology.

[19]  Charles L. Cox,et al.  Glutamate Inhibits Thalamic Reticular Neurons , 1999, The Journal of Neuroscience.

[20]  Mark W. Woolrich,et al.  Attention to touch modulates activity in both primary and secondary somatosensory areas. , 2000 .

[21]  Ellen Perecman,et al.  The frontal lobes revisited. , 1987 .

[22]  R W Cox,et al.  Real‐Time Functional Magnetic Resonance Imaging , 1995, Magnetic resonance in medicine.

[23]  V. M. Montero,et al.  C-fos induction in sensory pathways of rats exploring a novel complex environment: shifts of active thalamic reticular sectors by predominant sensory cues , 1997, Neuroscience.

[24]  H Burton,et al.  Tactile attention tasks enhance activation in somatosensory regions of parietal cortex: a positron emission tomography study. , 1999, Cerebral cortex.

[25]  D B Plewes,et al.  New devices to deliver somatosensory stimuli during functional MRI , 2001, Magnetic resonance in medicine.

[26]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[27]  S. Nakamura,et al.  Pyramidal tract control over cutaneous and kinesthetic sensory transmission in the cat thalamus , 1975, Experimental Brain Research.

[28]  Kerry McAlonan,et al.  Thalamic Reticular Nucleus Activation Reflects Attentional Gating during Classical Conditioning , 2000, The Journal of Neuroscience.

[29]  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.

[30]  W. Jiang,et al.  Modulation of lemniscal input during conditioned arm movements in the monkey , 2004, Experimental Brain Research.

[31]  A. Canedo PRIMARY MOTOR CORTEX INFLUENCES ON THE DESCENDING AND ASCENDING SYSTEMS , 1997, Progress in Neurobiology.

[32]  Y. Iwamura,et al.  Bilateral receptive field neurons and callosal connections in the somatosensory cortex. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[33]  A. Siegel,et al.  Effect of stimulation of prefrontal cortex and amygdala on diencephalic neurons , 1975, Brain Research.

[34]  G. E. Alexander,et al.  Convergence of prefrontal and acoustic inputs upon neurons in the superior temporal gyrus of the awake squirrel monkey , 1976, Brain Research.

[35]  E. G. Jones,et al.  Distribution of callosal fibers around the hand representations in monkey somatic sensory cortex , 1980, Neuroscience Letters.

[36]  James E. Skinner,et al.  Central Gating Mechanisms That Regulate Event-Related Potentials and Behavior , 1984 .

[37]  M. Raichle,et al.  Blood flow changes in human somatosensory cortex during anticipated stimulation , 1995, Nature.

[38]  K. Meador,et al.  Functional MRI cerebral activation and deactivation during finger movement , 2000, Neurology.

[39]  Leah Krubitzer,et al.  Interhemispheric connections of somatosensory cortex in the flying fox , 1998, The Journal of comparative neurology.

[40]  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 .