Force sensor in simulated skin and neural model mimic tactile SAI afferent spiking response to ramp and hold stimuli

BackgroundThe next generation of prosthetic limbs will restore sensory feedback to the nervous system by mimicking how skin mechanoreceptors, innervated by afferents, produce trains of action potentials in response to compressive stimuli. Prior work has addressed building sensors within skin substitutes for robotics, modeling skin mechanics and neural dynamics of mechanotransduction, and predicting response timing of action potentials for vibration. The effort here is unique because it accounts for skin elasticity by measuring force within simulated skin, utilizes few free model parameters for parsimony, and separates parameter fitting and model validation. Additionally, the ramp-and-hold, sustained stimuli used in this work capture the essential features of the everyday task of contacting and holding an object.MethodsThis systems integration effort computationally replicates the neural firing behavior for a slowly adapting type I (SAI) afferent in its temporally varying response to both intensity and rate of indentation force by combining a physical force sensor, housed in a skin-like substrate, with a mathematical model of neuronal spiking, the leaky integrate-and-fire. Comparison experiments were then conducted using ramp-and-hold stimuli on both the spiking-sensor model and mouse SAI afferents. The model parameters were iteratively fit against recorded SAI interspike intervals (ISI) before validating the model to assess its performance.ResultsModel-predicted spike firing compares favorably with that observed for single SAI afferents. As indentation magnitude increases (1.2, 1.3, to 1.4 mm), mean ISI decreases from 98.81 ± 24.73, 54.52 ± 6.94, to 41.11 ± 6.11 ms. Moreover, as rate of ramp-up increases, ISI during ramp-up decreases from 21.85 ± 5.33, 19.98 ± 3.10, to 15.42 ± 2.41 ms. Considering first spikes, the predicted latencies exhibited a decreasing trend as stimulus rate increased, as is observed in afferent recordings. Finally, the SAI afferent’s characteristic response of producing irregular ISIs is shown to be controllable via manipulating the output filtering from the sensor or adding stochastic noise.ConclusionsThis integrated engineering approach extends prior works focused upon neural dynamics and vibration. Future efforts will perfect measures of performance, such as first spike latency and irregular ISIs, and link the generation of characteristic features within trains of action potentials with current pulse waveforms that stimulate single action potentials at the peripheral afferent.

[1]  G. J. Gerling,et al.  The regularity of sustained firing reveals two populations of slowly adapting touch receptors in mouse hairy skin. , 2010, Journal of neurophysiology.

[2]  Kathryn Ziegler-Graham,et al.  Estimating the prevalence of limb loss in the United States: 2005 to 2050. , 2008, Archives of physical medicine and rehabilitation.

[3]  Robert D. Howe,et al.  A holistic model of human touch , 1997 .

[4]  G.S. Dhillon,et al.  Direct neural sensory feedback and control of a prosthetic arm , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[5]  Sliman Bensmaïa A transduction model of the Meissner corpuscle. , 2002, Mathematical biosciences.

[6]  A. W. Schopper,et al.  A structural fingertip model for simulating of the biomechanics of tactile sensation. , 2004, Medical engineering & physics.

[7]  S. W. Kuffler,et al.  From Neuron to Brain: A Cellular and Molecular Approach to the Function of the Nervous System , 1992 .

[8]  Kazumi Kobayashi,et al.  Relationship between the Structure of Human Finger Tissue and the Location of Tactile Receptors , 1998 .

[9]  G. Debrégeas,et al.  The Role of Fingerprints in the Coding of Tactile Information Probed with a Biomimetic Sensor , 2009, Science.

[10]  D Popović,et al.  Perspectives on the role of afferent signals in control of motor neuroprostheses. , 1995, Medical engineering & physics.

[11]  Mark H. Lee,et al.  Tactile Sensing: New Directions, New Challenges , 2000, Int. J. Robotics Res..

[12]  G. J. Gerling,et al.  Fingerprint lines may not directly affect SA-I mechanoreceptor response , 2008, Somatosensory & motor research.

[13]  P. Khalsa,et al.  Encoding of compressive stress during indentation by slowly adapting type I mechanoreceptors in rat hairy skin. , 2002, Journal of neurophysiology.

[14]  R. Johansson,et al.  First spikes in ensembles of human tactile afferents code complex spatial fingertip events , 2004, Nature Neuroscience.

[15]  S S Hsiao,et al.  Vibratory adaptation of cutaneous mechanoreceptive afferents. , 2005, Journal of neurophysiology.

[16]  P. Matthews,et al.  Active touch—the mechanism of recognition of objects by manipulation: A multidisciplinary approach G. Gordon(Ed.) Pergamon, Oxford. 288 pp., $22.00. paper; $38.50 hardback , 1979, Neuroscience.

[17]  Kenneth O. Johnson,et al.  A continuum mechanical model of mechanoreceptive afferent responses to indented spatial patterns. , 2006, Journal of neurophysiology.

[18]  D. C. Higgins Touch, Heat and Pain , 1967, The Yale Journal of Biology and Medicine.

[19]  Christian Cipriani,et al.  The SmartHand transradial prosthesis , 2011, Journal of NeuroEngineering and Rehabilitation.

[20]  K W Horch,et al.  Impulse generation in type I cutaneous mechanoreceptors. , 1974, Journal of neurophysiology.

[21]  Vernon B. Mountcastle,et al.  The Neural Transformation of Mechanical Stimuli Delivered to the Monkey's Hand , 2008 .

[22]  G. J. Gerling,et al.  Predicting SA-I mechanoreceptor spike times with a skin-neuron model. , 2009, Mathematical biosciences.

[23]  Z. Ounaiesa,et al.  Electrical properties of single wall carbon nanotube reinforced polyimide composites , 2003 .

[24]  Sung Soo Kim,et al.  Conveying Tactile Feedback in Sensorized Hand Neuroprostheses Using a Biofidelic Model of Mechanotransduction , 2009, IEEE Transactions on Biomedical Circuits and Systems.

[25]  A. R. Muir,et al.  The structure and function of a slowly adapting touch corpuscle in hairy skin , 1969, The Journal of physiology.

[26]  K. O. Johnson,et al.  Tactile spatial resolution. III. A continuum mechanics model of skin predicting mechanoreceptor responses to bars, edges, and gratings. , 1981, Journal of neurophysiology.

[27]  Silvestro Micera,et al.  On the identification of sensory information from mixed nerves by using single-channel cuff electrodes , 2009, Journal of NeuroEngineering and Rehabilitation.

[28]  B. H. Pubols Factors affecting cutaneous mechanoreceptor response. II. Changes in mechanical properties of skin with repeated stimulation. , 1982, Journal of neurophysiology.

[29]  Balasundar I Raju,et al.  3-D finite-element models of human and monkey fingertips to investigate the mechanics of tactile sense. , 2003, Journal of biomechanical engineering.

[30]  Eugene M. Izhikevich,et al.  Simple model of spiking neurons , 2003, IEEE Trans. Neural Networks.

[31]  Kenneth O. Johnson,et al.  The roles and functions of cutaneous mechanoreceptors , 2001, Current Opinion in Neurobiology.

[32]  Alex M. Andrew,et al.  Spiking Neuron Models: Single Neurons, Populations, Plasticity , 2003 .

[33]  G. J. Gerling,et al.  Skin relaxation predicts neural firing rate adaptation in SAI touch receptors , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[34]  Masatoshi Ishikawa,et al.  Development of a system for experiencing tactile sensation from a robot hand by electrically stimulating sensory nerve fiber , 2003, 2003 IEEE International Conference on Robotics and Automation (Cat. No.03CH37422).

[35]  Naoki Kawakami,et al.  Finger-Shaped GelForce: Sensor for Measuring Surface Traction Fields for Robotic Hand , 2010, IEEE Transactions on Haptics.

[36]  D P Corey,et al.  Two mechanisms for transducer adaptation in vertebrate hair cells. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  B H Pubols Factors affecting cutaneous mechanoreceptor response. I. Constant-force versus constant-displacement stimulation. , 1982, Journal of neurophysiology.

[38]  K. Rajanna,et al.  Tactile sensor based on piezoelectric resonance , 2002, Proceedings of IEEE Sensors.

[39]  M. Aminoff Principles of Neural Science. 4th edition , 2001 .

[40]  R. Etienne-Cummings,et al.  Real-time implementation of biofidelic SA1 model for tactile feedback , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[41]  M. Srinivasan,et al.  An investigation of the mechanics of tactile sense using two-dimensional models of the primate fingertip. , 1996, Journal of biomechanical engineering.

[42]  J. Rothwell Principles of Neural Science , 1982 .

[43]  Luca Citi,et al.  Decoding of grasping information from neural signals recorded using peripheral intrafascicular interfaces , 2011, Journal of NeuroEngineering and Rehabilitation.