Cognitive Load Can Explain Differences in Active and Passive Touch

Active touch is often described as yielding "better-quality" information than passive touch. However, some authors have argued that passive-guided movements generate superior percepts due to a reduction in demands on the haptic sensory system. We consider the possibility that passive-guided conditions, as used in most active-passive comparisons, are relatively free from cognitive decision-making, while active conditions involve cognitive loads that are quite high and uncharacteristic of normal sensory processes. Thus studies that purport to show differences in active and passive touch may instead be revealing differences in the amount of cognition involved in active and passive tasks. We hypothesized that passive-guided conditions reduce not the sensory load but the cognitive load that active explorers must bear. To test this hypothesis Blood Oxygen Level Dependent (BOLD) activity was measured using functional Magnetic Resonance Imaging (fMRI) during active and passive-guided fingertip exploration of 2D raised line drawings. Active movements resulted in greater activation (compared with passive movements) in areas implicated in higher order processes such as monitoring and controlling of goal-directed behavior, attention, execution of movements, and error detection. Passive movements, in contrast, produced greater BOLD activity in areas associated with touch perception, length discrimination, tactile object recognition, and efference copy. The activation of a greater number of higher-order processing areas during active relative to passive-guided exploration suggests that instances of passive-guided superiority may not be due to the haptic system's limited ability to cope with sensory inputs, but rather the restriction imposed by the use of a single finger such that active exploration may require cognitive strategies not demanded in the passive condition. Our findings suggest that previous attempts to compare active and passive touch have, in order to simplify tasks, inadvertently introduced cognitive load at the expense of normal sensory inputs.

[1]  D. Brooks The role of the basal ganglia in motor control: contributions from PET , 1995, Journal of the Neurological Sciences.

[2]  Soledad Ballesteros,et al.  Touch, blindness, and neuroscience , 2004 .

[3]  S. Kiebel,et al.  Brain Representation of Active and Passive Movements , 1996, NeuroImage.

[4]  Geraint Rees,et al.  The Cutaneous Rabbit Illusion Affects Human Primary Sensory Cortex Somatotopically , 2006, PLoS biology.

[5]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

[6]  Michael D. Rugg,et al.  Effects of Age on the Neural Correlates of Retrieval Cue Processing are Modulated by Task Demands , 2009, Journal of Cognitive Neuroscience.

[7]  T. Mima,et al.  Brain structures related to active and passive finger movements in man. , 1999, Brain : a journal of neurology.

[8]  D. Schacter,et al.  A sensory signature that distinguishes true from false memories , 2004, Nature Neuroscience.

[9]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[10]  Noam Sobel,et al.  Attentional modulation in human primary olfactory cortex , 2005, Nature Neuroscience.

[11]  P. Roland,et al.  Activity in the human primary motor cortex related to ipsilateral hand movements , 1994, Brain Research.

[12]  Joshua W. Brown,et al.  Conflict effects without conflict in anterior cingulate cortex: Multiple response effects and context specific representations , 2009, NeuroImage.

[13]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[14]  P. Matthews,et al.  Altered cortical activation with finger movement after peripheral denervation: comparison of active and passive tasks , 2001, NeuroImage.

[15]  J. Kennedy,et al.  Exploring pictures tactually , 1980, Nature.

[16]  R. Klatzky,et al.  Do intention and exploration modulate the pathways to haptic object identification? , 2007, Behavioral and Brain Sciences.

[17]  J. Bower,et al.  Cerebellum Implicated in Sensory Acquisition and Discrimination Rather Than Motor Control , 1996, Science.

[18]  M. Barinaga The Cerebellum: Movement Coordinator or Much More? , 1996, Science.

[19]  J. Decety,et al.  Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta‐analysis , 2001, Human brain mapping.

[20]  B L Richardson,et al.  Can passive touch be better than active touch? A comparison of active and passive tactile maze learning. , 1981, British journal of psychology.

[21]  J. Tanji,et al.  Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. , 1998, Journal of neurophysiology.

[22]  Joshua W. Brown,et al.  Learned Predictions of Error Likelihood in the Anterior Cingulate Cortex , 2005, Science.

[23]  Philip Servos,et al.  The influence of familiarity on brain activation during haptic exploration of 3-D facemasks , 2006, Neuroscience Letters.

[24]  BARRY L. RICHARDSON,et al.  Can passive tactile perception be better than active? , 1981, Nature.

[25]  N. Kanwisher,et al.  The lateral occipital complex and its role in object recognition , 2001, Vision Research.

[26]  J. Gibson Observations on active touch. , 1962, Psychological review.

[27]  Karl J. Friston,et al.  Regional cerebral blood flow during voluntary arm and hand movements in human subjects. , 1991, Journal of neurophysiology.

[28]  R. Thangavel,et al.  Modular and laminar pathology of Brodmann’s area 37 in Alzheimer’s disease , 2008, Neuroscience.

[29]  J. Nielsen,et al.  Premotor cortex modulates somatosensory cortex during voluntary movements without proprioceptive feedback , 2007, Nature Neuroscience.

[30]  K O Johnson,et al.  A comparison of visual and two modes of tactual letter resolution , 1983, Perception & psychophysics.

[31]  Stephen M. Rao,et al.  Neural Basis of Endogenous and Exogenous Spatial Orienting: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[32]  C. Frith,et al.  How do we predict the consequences of our actions? a functional imaging study , 1998, Neuropsychologia.

[33]  S. Blakemore,et al.  Delusions of alien control in the normal brain , 2003, Neuropsychologia.

[34]  John W. Thatcher,et al.  Putamen coactivation during motor task execution , 2008, Neuroreport.

[35]  R. Passingham,et al.  Functional anatomy of the mental representation of upper extremity movements in healthy subjects. , 1995, Journal of neurophysiology.

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

[37]  Jason B. Mattingley,et al.  Motor role of human inferior parietal lobe revealed in unilateral neglect patients , 1998, Nature.

[38]  Susan J. Lederman,et al.  Functional Specialization and Convergence in the Occipito-temporal Cortex Supporting Haptic and Visual Identification of Human Faces and Body Parts: An fMRI Study , 2009, Journal of Cognitive Neuroscience.

[39]  Mark A Symmons,et al.  Components of Haptic Information: Skin Rivals Kinaesthesis , 2008, Perception.

[40]  M. Raichle,et al.  Localization of a human system for sustained attention by positron emission tomography , 1991, Nature.

[41]  D. Wolpert,et al.  Sensorimotor attenuation by central motor command signals in the absence of movement , 2006, Nature Neuroscience.

[42]  C. Büchel,et al.  Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. , 1997, Cerebral cortex.