Task-specific increase in corticomotor excitability during tactile discrimination

Task-dependant changes in corticomotor excitability have been described mainly in the context of grasp-oriented actions, neglecting the sensory aspects of hand function. Here, we contrasted task-dependant facilitation in small hand muscles [i.e., first dorsal interosseous (FDI) and abductor digiti minimi (ADM)] in the context of finger movements involving either discrimination or non discrimination (ND) of tactile features. Healthy young individuals (n = 16) were trained to produce rhythmic to and fro movements at the sound of metronome ticks (0.8 Hz frequency, 5 s total duration) with either the index or the little finger of the right hand. In the tactile discrimination (TD) condition, participants were asked to attend to the location of two different 2-D tactile shapes disposed on the explored surface, whereas in the ND condition, the finger was moved over a blank surface. In both conditions, a transcranial magnetic stimulation (TMS) pulse was delivered at a specific time point in the course of the finger movement. Corticomotor excitability was assessed by monitoring changes in the amplitude and latency of motor evoked potentials (MEPs) in the FDI and ADM. Changes in the duration of the silent period were also assessed. The analysis revealed a significant large effect of task conditions (P < 0.001) on MEP amplitude, owing to the increase in MEP size observed during the TD, as compared to the ND condition. No interaction between “Task” and “Muscle” was detected, however, indicating that MEPs in the two muscles were equally affected by the task conditions. No significant changes were detected for variations in MEP latency or in the SP duration. An additional control experiment performed in a subset of the participants (n = 9) showed that MEP facilitation was substantially reduced when attention to sensations arising from finger contact with the shapes was diverted away by completion of a concurrent cognitive task (counting backward by three). These findings provide further insights into the factors influencing task-dependant changes in corticomotor excitability during hand actions. Our results highlight the importance of behavioral context and attention, in particular, in leading to further enhancement in corticomotor excitability when the finger is actively engaged in TD.

[1]  Y. Ohki,et al.  Cutaneous inputs can activate the ipsilateral primary motor cortex during bimanual sensory-driven movements in humans. , 2004, Journal of neurophysiology.

[2]  J. Honoré,et al.  Effects of spatially oriented attention on the facilitation of the H reflex by a cutaneous stimulus. , 1983, Electroencephalography and clinical neurophysiology.

[3]  T. Tsuji,et al.  Functional demanded excitability changes of human hand motor area , 2006, Experimental Brain Research.

[4]  Karl J. Friston,et al.  Attention to Action: Specific Modulation of Corticocortical Interactions in Humans , 2001, NeuroImage.

[5]  K. Mills,et al.  Corticomotor threshold to magnetic stimulation: Normal values and repeatability , 1997, Muscle & nerve.

[6]  J. Nielsen,et al.  Logarithmic distribution of amplitudes of compound muscle action potentials evoked by transcranial magnetic stimulation. , 1996, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[7]  Kenneth O. Johnson,et al.  Tactile Functions of Mechanoreceptive Afferents Innervating the Hand , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[8]  E. Kunesch,et al.  Task-dependent modulation of inhibitory actions within the primary motor cortex , 1999, Experimental Brain Research.

[9]  M Schieppati,et al.  Selective facilitation of responses to cortical stimulation of proximal and distal arm muscles by precision tasks in man. , 1996, The Journal of physiology.

[10]  K. Sathian,et al.  Tactile spatial acuity at the human fingertip and lip , 1996, Neurology.

[11]  M. Roth,et al.  Neuronal substrates of haptic shape encoding and matching: A functional magnetic resonance imaging study , 2008, Neuroscience.

[12]  Mizuo Kimura,et al.  Amplitude reduction of H-reflex during mental movement simulation in elite athletes , 1994, Behavioural Brain Research.

[13]  T. Tsuji,et al.  Motor strategies and excitability changes of human hand motor area are dependent on different voluntary drives , 2006, The European journal of neuroscience.

[14]  J. Rothwell,et al.  The effect of sensory input and attention on the sensorimotor organization of the hand area of the human motor cortex , 2004, The Journal of physiology.

[15]  Erhard J. Huesler,et al.  Task dependence of muscle synchronization in human hand muscles , 1998, Neuroreport.

[16]  J. Summers,et al.  Attentional influences on short-interval intracortical inhibition , 2008, Clinical Neurophysiology.

[17]  M H Schieber,et al.  Quantifying the Independence of Human Finger Movements: Comparisons of Digits, Hands, and Movement Frequencies , 2000, The Journal of Neuroscience.

[18]  Minming Zhang,et al.  Neural networks active during tactile form perception: common and differential activity during macrospatial and microspatial tasks. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[19]  Susan J. Lederman,et al.  Extracting object properties through haptic exploration. , 1993, Acta psychologica.

[20]  K. Zilles,et al.  Hierarchical Processing of Tactile Shape in the Human Brain , 2001, Neuron.

[21]  M. Bonnard,et al.  Corticospinal control of the thumb–index grip depends on precision of force control: a transcranial magnetic stimulation and functional magnetic resonance imagery study in humans , 2007, The European journal of neuroscience.

[22]  Kenneth O. Johnson,et al.  Neural Coding Mechanisms Underlying Perceived Roughness of Finely Textured Surfaces , 2001, The Journal of Neuroscience.

[23]  A. Berardelli,et al.  Attention influences the excitability of cortical motor areas in healthy humans , 2007, Experimental Brain Research.

[24]  Ovidiu Lungu,et al.  Primary Motor Area Activation during Precision-Demanding versus Simple Finger Movement , 2006, Neurorehabilitation and neural repair.

[25]  K. Mills,et al.  Cortical and spinal mechanisms of facilitation to brain stimulation , 1996, Muscle & nerve.

[26]  Marc H Schieber,et al.  Hand function: peripheral and central constraints on performance. , 2004, Journal of applied physiology.

[27]  原田 宗子,et al.  Asymmetrical neural substrates of tactile discrimination in humans : a functional magnetic resonance imaging study , 2005 .

[28]  H. Kinoshita,et al.  Modulation of a motor evoked response to transcranial magnetic stimulation by the activity level of the first dorsal interosseous muscle in humans when grasping a stationary object with different grip widths , 2001, Neuroscience Letters.

[29]  Giovanni Abbruzzese,et al.  Clinical and Research Methods for Evaluating Cortical Excitability , 2002, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[30]  Shozo Tobimatsu,et al.  Different patterns of excitation and inhibition of the small hand and forearm muscles from magnetic brain stimulation in humans , 2002, Clinical Neurophysiology.

[31]  R. Lemon,et al.  Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. , 1986, The Journal of physiology.

[32]  L M Harrison,et al.  Task‐dependent changes in the size of response to magnetic brain stimulation in human first dorsal interosseous muscle. , 1989, The Journal of physiology.

[33]  P. Strick,et al.  Motor areas in the frontal lobe of the primate , 2002, Physiology & Behavior.

[34]  R N Lemon,et al.  Task dependence of responses in first dorsal interosseous muscle to magnetic brain stimulation in man. , 1993, The Journal of physiology.