Increasing top-down suppression from prefrontal cortex facilitates tactile working memory

Navigated transcranial magnetic stimulation (TMS) combined with diffusion-weighted magnetic resonance imaging (DW-MRI) and tractography allows investigating functional anatomy of the human brain with high precision. Here we demonstrate that working memory (WM) processing of tactile temporal information is facilitated by delivering a single TMS pulse to the middle frontal gyrus (MFG) during memory maintenance. Facilitation was obtained only with a TMS pulse applied to a location of the MFG with anatomical connectivity to the primary somatosensory cortex (S1). TMS improved tactile WM also when distractive tactile stimuli interfered with memory maintenance. Moreover, TMS to the same MFG site attenuated somatosensory evoked responses (SEPs). The results suggest that the TMS-induced memory improvement is explained by increased top-down suppression of interfering sensory processing in S1 via the MFG-S1 link. These results demonstrate an anatomical and functional network that is involved in maintenance of tactile temporal WM.

[1]  S. Boniface,et al.  Magnetic brain stimulation with a double coil: the importance of coil orientation. , 1992, Electroencephalography and clinical neurophysiology.

[2]  J. Fuster.  Prefrontal Cortex , 2018 .

[3]  R. Passingham,et al.  Active maintenance in prefrontal area 46 creates distractor-resistant memory , 2002, Nature Neuroscience.

[4]  P Rämä,et al.  Selective interference reveals dissociation between auditory memory for location and pitch. , 1999, Neuroreport.

[5]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

[6]  R. Romo,et al.  Temporal Evolution of a Decision-Making Process in Medial Premotor Cortex , 2002, Neuron.

[7]  R Salmelin,et al.  The 3D topography of MEG source localization accuracy: effects of conductor model and noise , 2003, Clinical Neurophysiology.

[8]  P. Goldman-Rakic,et al.  Connections of the ventral granular frontal cortex of macaques with perisylvian premotor and somatosensory areas: Anatomical evidence for somatic representation in primate frontal association cortex , 1989, The Journal of comparative neurology.

[9]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[10]  Stephen J. Jones,et al.  Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve. A review of scalp and intracranial recordings. , 1991, Brain : a journal of neurology.

[11]  Emilio Salinas,et al.  Cognitive neuroscience: Flutter Discrimination: neural codes, perception, memory and decision making , 2003, Nature Reviews Neuroscience.

[12]  R. Knight,et al.  Contribution of Human Prefrontal Cortex to Delay Performance , 1998, Journal of Cognitive Neuroscience.

[13]  Riitta Salmelin,et al.  Cortical activation during a spatiotemporal tactile comparison task , 2004, NeuroImage.

[14]  F. Binkofski,et al.  Cerebral correlates of working memory for temporal information , 2000, NeuroReport.

[15]  Masud Seyal,et al.  Transcranial magnetic stimulation of left prefrontal cortex impairs working memory , 2001, Clinical Neurophysiology.

[16]  Timothy Edward John Behrens,et al.  Probabilistic diffusion tractography: a potential tool to assess the rate of disease progression in amyotrophic lateral sclerosis. , 2006, Brain : a journal of neurology.

[17]  M. Horsfield,et al.  Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging , 1999, Magnetic resonance in medicine.

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

[19]  R. Dell’Acqua,et al.  The Demonstration of Short-Term Consolidation , 1998, Cognitive Psychology.

[20]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

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

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

[23]  P Rämä,et al.  Selective interference reveals dissociation between memory for location and colour. , 1999, Neuroreport.

[24]  O. Salonen,et al.  Navigated transcranial magnetic stimulation of the primary somatosensory cortex impairs perceptual processing of tactile temporal discrimination , 2008, Neuroscience Letters.

[25]  R. Romo,et al.  Neuronal correlates of decision-making in secondary somatosensory cortex , 2002, Nature Neuroscience.

[26]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[27]  Justin A. Harris,et al.  Transient Storage of a Tactile Memory Trace in Primary Somatosensory Cortex , 2002, The Journal of Neuroscience.

[28]  Emilio Salinas,et al.  Discrimination in the Sense of Flutter: New Psychophysical Measurements in Monkeys , 1997, The Journal of Neuroscience.

[29]  J. Fuster,et al.  Visuo-tactile cross-modal associations in cortical somatosensory cells. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. J. Ilmoniemi,et al.  Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation , 1999, Medical & Biological Engineering & Computing.

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

[32]  G. Woodman,et al.  The time course of consolidation in visual working memory. , 2006, Journal of experimental psychology. Human perception and performance.

[33]  Theo G. M. van Erp,et al.  Diffusion Tensor Imaging of the Superior Longitudinal Fasciculus and Working Memory in Recent-Onset Schizophrenia , 2008, Biological Psychiatry.

[34]  Antti Korvenoja,et al.  Somatotopic blocking of sensation with navigated transcranial magnetic stimulation of the primary somatosensory cortex , 2005, Human brain mapping.

[35]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[36]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[37]  Jeffrey W. Cooney,et al.  Top-down suppression deficit underlies working memory impairment in normal aging , 2005, Nature Neuroscience.

[38]  R. Knight,et al.  Human prefrontal lesions increase distractibility to irrelevant sensory inputs , 1995, Neuroreport.

[39]  F. Plum.  Handbook of Physiology. , 1960 .

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

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

[42]  F. Awiszus.  TMS and threshold hunting. , 2003, Supplements to Clinical neurophysiology.

[43]  Bradley R. Postle,et al.  Delay-period Activity in the Prefrontal Cortex: One Function Is Sensory Gating , 2005, Journal of Cognitive Neuroscience.

[44]  C Tomberg,et al.  Mapping somatosensory evoked potentials to finger stimulation at intervals of 450 to 4000 msec and the issue of habituation when assessing early cognitive components. , 1989, Electroencephalography and clinical neurophysiology.

[45]  J. Sarvas.  Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. , 1987, Physics in medicine and biology.

[46]  Alvaro Pascual-Leone,et al.  Handbook of transcranial magnetic stimulation , 2002 .

[47]  R. Malmo.  INTERFERENCE FACTORS IN DELAYED RESPONSE IN MONKEYS AFTER REMOVAL OF FRONTAL LOBES , 1942 .

[48]  R. Romo,et al.  Periodicity and Firing Rate As Candidate Neural Codes for the Frequency of Vibrotactile Stimuli , 2000, The Journal of Neuroscience.

[49]  Michael X. Cohen,et al.  Working Memory Maintenance Contributes to Long-term Memory Formation: Neural and Behavioral Evidence , 2005, Journal of Cognitive Neuroscience.

[50]  R. Romo,et al.  Neuronal Correlates of a Perceptual Decision in Ventral Premotor Cortex , 2004, Neuron.

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

[52]  J. Fuster,et al.  Mnemonic neuronal activity in somatosensory cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.