Flexible multielectrodes can resolve multiple muscles in an insect appendage

Research into the neuromechanical basis of behavior, either in biomechanics, neuroethology, or neuroscience, is frequently limited by methods of data collection. Two of the most pressing needs are for methods with which to (1) record from multiple neurons or muscles simultaneously and (2) perform this recording in intact, behaving animals. In this paper we present the fabrication and testing of flexible multielectrode arrays (fMEAs) that move us significantly towards these goals. The fMEAs were used to record the activity of several distinct units in the coxa of the cockroach Blaberus discoidalis. The devices fabricated here address the first goal in two ways: (1) their flexibility allows them to be inserted into an animal and guided through internal tissues in order to access distinct groups of neurons and muscles and (2) their recording site geometry has been tuned to suit the anatomy under study, yielding multichannel spike waveforms that are easily separable under conditions of spike overlap. The flexible nature of the devices simultaneously addresses the second goal, in that it is less likely to interfere with the natural movement of the animal.

[1]  N. Trayanova,et al.  Extracellular potentials and currents of a single active fiber in a restricted volume conductor , 2006, Annals of Biomedical Engineering.

[2]  R. Ritzmann,et al.  Kinematics and motor activity during tethered walking and turning in the cockroach, Blaberus discoidalis , 2005, Journal of Comparative Physiology A.

[3]  Philip Holmes,et al.  Dynamics and stability of insect locomotion: a hexapedal model for horizontal plane motions , 2004, Biological Cybernetics.

[4]  T. Stieglitz,et al.  Flexible BIOMEMS with Electrode Arrangements on Front and Back Side as Key Component in Neural Prostheses and Biohybrid Systems , 2002 .

[5]  H. Cruse,et al.  Behaviour-based modelling of hexapod locomotion: linking biology and technical application. , 2004, Arthropod structure & development.

[6]  Isao Shimoyama,et al.  A radio-telemetry system with a shape memory alloy microelectrode for neural recording of freely moving insects , 2004, IEEE Transactions on Biomedical Engineering.

[7]  R. Full,et al.  Mechanical aspects of legged locomotion control. , 2004, Arthropod structure & development.

[8]  A. Kralj,et al.  Functional Electrical Stimulation: Standing and Walking after Spinal Cord Injury , 1989 .

[9]  B. McNaughton,et al.  Independent Codes for Spatial and Episodic Memory in Hippocampal Neuronal Ensembles , 2005, Science.

[10]  Michael J. Berry,et al.  Adaptation of retinal processing to image contrast and spatial scale , 1997, Nature.

[11]  Luca Berdondini,et al.  A microelectrode array (MEA) integrated with clustering structures for investigating in vitro neurodynamics in confined interconnected sub-populations of neurons , 2006 .

[12]  W. Kutsch,et al.  Transmission of muscle potentials during free flight of locusts , 2002 .

[13]  R J Full,et al.  Templates and anchors: neuromechanical hypotheses of legged locomotion on land. , 1999, The Journal of experimental biology.

[14]  U. Bässler,et al.  Pattern generation for stick insect walking movements—multisensory control of a locomotor program , 1998, Brain Research Reviews.

[15]  R. Full,et al.  A motor and a brake: two leg extensor muscles acting at the same joint manage energy differently in a running insect. , 2002, The Journal of experimental biology.

[16]  R Kanzaki,et al.  A dual-channel FM transmitter for acquisition of flight muscle activities from the freely flying hawkmoth, Agrius convolvuli , 2002, Journal of Neuroscience Methods.

[17]  J. Hildebrand,et al.  Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles , 2000, Nature Neuroscience.

[18]  E Marder,et al.  Modulation of Oscillator Interactions in the Crab Stomatogastric Ganglion by Crustacean Cardioactive Peptide , 1997, The Journal of Neuroscience.

[19]  R A Normann,et al.  Trial-by-trial discrimination of three enantiomer pairs by neural ensembles in mammalian olfactory bulb. , 2006, Journal of neurophysiology.

[20]  J. Miller,et al.  Information theoretic analysis of dynamical encoding by four identified primary sensory interneurons in the cricket cercal system. , 1996, Journal of neurophysiology.

[21]  Bruce R. Johnson,et al.  Tools for physiology labs: an inexpensive high-performance amplifier and electrode for extracellular recording , 2001, Journal of Neuroscience Methods.

[22]  D. W. Smith,et al.  Mechanics of slope walking in the cat: quantification of muscle load, length change, and ankle extensor EMG patterns. , 2006, Journal of neurophysiology.

[23]  E. Marder,et al.  Principles of rhythmic motor pattern generation. , 1996, Physiological reviews.

[24]  J. Weiland,et al.  Retinal prosthesis for the blind. , 2002, Survey of ophthalmology.

[25]  Conrad D. James,et al.  Extracellular recordings from patterned neuronal networks using planar microelectrode arrays , 2004, IEEE Transactions on Biomedical Engineering.

[26]  U. Bässler The femur-tibia control system of stick insects — a model system for the study of the neural basis of joint control , 1993, Brain Research Reviews.

[27]  B. Jayne,et al.  In vivo muscle activity in the hindlimb of the arboreal lizard, Chamaeleo calyptratus: general patterns and the effects of incline , 2004, Journal of Experimental Biology.

[28]  S. Grillner,et al.  Activity of reticulospinal neurons during locomotion in the freely behaving lamprey. , 2000, Journal of neurophysiology.

[29]  K G Pearson,et al.  Connexions between hair-plate afferents and motoneurones in the cockroach leg. , 1976, The Journal of experimental biology.

[30]  C. S. Carbonell The thoracic muscles of the cockroach Periplaneta americana (L.) , 1947 .

[31]  Philip Holmes,et al.  A Simply Stabilized Running Model , 2005, SIAM Rev..

[32]  Silvestro Micera,et al.  A critical review of interfaces with the peripheral nervous system for the control of neuroprostheses and hybrid bionic systems , 2005, Journal of the peripheral nervous system : JPNS.

[33]  X. Navarro,et al.  Noninvasive measurement of torque development in the rat foot: measurement setup and results from stimulation of the sciatic nerve with polyimide-based cuff electrodes , 2003, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[34]  S. Zill,et al.  Common motor mechanisms support body load in serially homologous legs of cockroaches in posture and walking , 2006, Journal of Comparative Physiology A.

[35]  W. Gronenberg The fast mandible strike in the trap-jaw ant Odontomachus , 1995, Journal of Comparative Physiology A.

[36]  Raffaele M. Ghigliazza,et al.  TOWARDS A NEUROMECHANICAL MODEL FOR INSECT LOCOMOTION: HYBRID DYNAMICAL SYSTEMS , 2005 .

[37]  W. Gronenberg,et al.  The fast mandible strike in the trap-jaw ant Odontomachus , 1995, Journal of Comparative Physiology A.

[38]  D F Stegeman,et al.  A thin, flexible multielectrode grid for high-density surface EMG. , 2004, Journal of applied physiology.

[39]  Alexander Dimitrov,et al.  Characterization of and compensation for the nonstationarity of spike shapes during physiological recordings , 2001, Neurocomputing.

[40]  E. Valderrama,et al.  Polyimide cuff electrodes for peripheral nerve stimulation , 2000, Journal of Neuroscience Methods.

[41]  John Guckenheimer,et al.  The Dynamics of Legged Locomotion: Models, Analyses, and Challenges , 2006, SIAM Rev..

[42]  N. Lago,et al.  Long term assessment of axonal regeneration through polyimide regenerative electrodes to interface the peripheral nerve. , 2005, Biomaterials.

[43]  M. Frye,et al.  Visual receptive field properties of feature detecting neurons in the dragonfly , 1995, Journal of Comparative Physiology A.

[44]  Philip Holmes,et al.  A Minimal Model of a Central Pattern Generator and Motoneurons for Insect Locomotion , 2004, SIAM J. Appl. Dyn. Syst..

[45]  K.D. Wise,et al.  Silicon microsystems for neuroscience and neural prostheses , 2005, IEEE Engineering in Medicine and Biology Magazine.