Transient and steady-state responses to mechanical stimulation of different fingers reveal interactions based on lateral inhibition

OBJECTIVE Simultaneous tactile finger stimulation evokes transient ERP responses that are smaller than the linear summation of ERP responses to individual stimulation. Occlusion and lateral inhibition are two possible mechanisms responsible for this effect. The present study disentangles these two effects using steady-state somatosensory evoked potentials (SSSEP). Simultaneous stimulation on adjacent and distant finger pairs with the same and different stimulation frequencies are compared. METHODS The index finger (IF), middle finger (MF) and little finger (LF) were mechanically stimulated with a frequency of 18, 22 or 26Hz, respectively. Stimulation was applied for each finger separately, and for the IF (18Hz) in combination with either the MF or LF for 22 and 26Hz, respectively. A measure for interaction (IR) was calculated for the P60 component and the SSSEP amplitude. RESULTS Significant interactions were found in both the P60 response and in the SSSEP response. Stimulation of adjacent finger combinations caused more interaction than distant finger combinations. No difference was found between stimulation of two fingers with the same or a different frequency. CONCLUSIONS Our results indicate that lateral inhibition is mainly responsible for the interaction effect. SIGNIFICANCE These observations provide further insight in the mechanisms behind interaction between somatosensory inputs.

[1]  R. Romo,et al.  Frequency discrimination in the sense of flutter: psychophysical measurements correlated with postcentral events in behaving monkeys , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  R Kakigi,et al.  Influence of concurrent tactile stimulation on somatosensory evoked potentials following posterior tibial nerve stimulation in man. , 1986, Electroencephalography and clinical neurophysiology.

[3]  Alfons Schnitzler,et al.  Rapid mapping of finger representations in human primary somatosensory cortex applying neuromagnetic steady-state responses , 2002, Neuroreport.

[4]  G Cheron,et al.  Gating of the early components of the frontal and parietal somatosensory evoked potentials in different sensory-motor interference modalities. , 1991, Electroencephalography and clinical neurophysiology.

[5]  R Hari,et al.  Interaction of afferent impulses in the human primary sensorimotor cortex. , 1992, Electroencephalography and clinical neurophysiology.

[6]  G. Pfurtscheller,et al.  Steady-state somatosensory evoked potentials: suitable brain signals for brain-computer interfaces? , 2006, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[7]  Jürgen Konczak,et al.  Interaction of finger representation in the human first somatosensory cortex: a neuromagnetic study , 1998, Neuroscience Letters.

[8]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[9]  E. Favale,et al.  The effect of hand muscle vibration on the somatosensory evoked potential in man: an interaction between lemniscal and spinocerebellar inputs? , 1980, Journal of neurology, neurosurgery, and psychiatry.

[10]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[11]  Hand posture modulates neuronal interaction in the primary somatosensory cortex of humans , 2003, Clinical Neurophysiology.

[12]  Esther P. Gardner,et al.  Cortical Neuronal Mechanisms Underlying the Perception of Motion Across the Skin , 1984 .

[13]  Matthias M. Müller,et al.  Selective spatial attention to left or right hand flutter sensation modulates the steady-state somatosensory evoked potential. , 2004, Brain research. Cognitive brain research.

[14]  Yijun Wang,et al.  A Brain-Computer Interface Based on Multi-Modal Attention , 2007, 2007 3rd International IEEE/EMBS Conference on Neural Engineering.

[15]  Christoph Stippich,et al.  Interaction of Tactile Input in the Human Primary and Secondary Somatosensory Cortex—A Magnetoencephalographic Study , 2001, NeuroImage.

[16]  Shozo Tobimatsu,et al.  Steady-state vibration somatosensory evoked potentials: physiological characteristics and tuning function , 1999, Clinical Neurophysiology.

[17]  P. Z. Marmarelis,et al.  Analysis of Physiological Systems: The White-Noise Approach , 2011 .

[18]  B L Whitsel,et al.  Frequency-dependent response of SI RA-class neurons to vibrotactile stimulation of the receptive field. , 2001, Somatosensory & motor research.

[19]  G. Pfurtscheller,et al.  „Resonance-like“ Frequencies of Sensorimotor Areas Evoked by Repetitive Tactile Stimulation - Resonanzeffekte in sensomotorischen Arealen, evoziert durch rhythmische taktile Stimulation , 2001, Biomedizinische Technik. Biomedical engineering.

[20]  J. Hyvärinen,et al.  Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. , 1969, Journal of neurophysiology.

[21]  S. C. Gandevia,et al.  Convergence in the somatosensory pathway between cutaneous afferents from the index and middle fingers in man , 2004, Experimental Brain Research.

[22]  N Forss,et al.  Functional overlap of finger representations in human SI and SII cortices. , 2001, Journal of neurophysiology.

[23]  Riitta Hari,et al.  Interaction between afferent input from fingers in human somatosensory cortex , 1995, Brain Research.

[24]  H Suzuki,et al.  Effects of tactile interference stimulation on somatosensory evoked magnetic fields following tibial nerve stimulation. , 1996, Electroencephalography and clinical neurophysiology.

[25]  R Kakigi,et al.  Effects on median nerve SEPs of tactile stimulation applied to adjacent and remote areas of the body surface. , 1985, Electroencephalography and clinical neurophysiology.

[26]  Mark L Latash,et al.  Multifinger Prehension: An Overview , 2008, Journal of motor behavior.

[27]  S. Gielen,et al.  The brain–computer interface cycle , 2009, Journal of neural engineering.

[28]  R Kakigi,et al.  Ipsilateral and contralateral SEP components following median nerve stimulation: effects of interfering stimuli applied to the contralateral hand. , 1986, Electroencephalography and clinical neurophysiology.

[29]  Shozo Tobimatsu,et al.  Differential interaction of somatosensory inputs in the human primary sensory cortex: a magnetoencephalographic study , 2000, Clinical Neurophysiology.

[30]  F. Valldeoriola,et al.  Subcortical interactions between somatosensory stimuli of different modalities and their temporal profile. , 2008, Journal of neurophysiology.

[31]  A. Kimura,et al.  Interactions of somatosensory evoked potentials: simultaneous stimulation of two nerves. , 1991, Electroencephalography and clinical neurophysiology.

[32]  R. Ilmoniemi,et al.  Effects of interstimulus interval on somatosensory evoked magnetic fields (SEFs): a hypothesis concerning SEF generation at the primary sensorimotor cortex. , 1996, Electroencephalography and clinical neurophysiology.

[33]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[34]  Clemens Brunner,et al.  Proceedings of the 4th International Brain-Computer Interface Workshop and Training Course 2008 , 2008 .

[35]  Timothy Bardouille,et al.  MEG imaging of sensorimotor areas using inter-trial coherence in vibrotactile steady-state responses , 2008, NeuroImage.

[36]  S Tobimatsu,et al.  The interaction of the somatosensory evoked potentials to simultaneous finger stimuli in the human central nervous system. A study using direct recordings. , 1995, Electroencephalography and clinical neurophysiology.

[37]  Y. Haruta,et al.  Neural mechanisms for generation of tactile interference effects on somatosensory evoked magnetic fields in humans , 2002, Clinical Neurophysiology.

[38]  B. Whitsel,et al.  Response of anterior parietal cortex to cutaneous flutter versus vibration. , 1999, Journal of neurophysiology.

[39]  N Birbaumer,et al.  Multiple frequency steady-state evoked magnetic field mapping of digit representation in primary somatosensory cortex. , 2001, Somatosensory & motor research.