A neuromechanical simulation of insect walking and transition to turning of the cockroach Blaberus discoidalis

A neuromechanical simulation of the cockroach Blaberus discoidalis was developed to explore changes in locomotion when the animal transitions from walking straight to turning. The simulation was based upon the biological data taken from three sources. Neural circuitry was adapted from the extensive literature primarily obtained from the studies of neural connections within thoracic ganglia of stick insect and adapted to cockroach. The 3D joint kinematic data on straight, forward walking for cockroach were taken from a paper that describes these movements in all joints simultaneously as the cockroach walked on an oiled-plate tether (Bender et al. in PloS one 5(10):1–15, 2010b). Joint kinematics for turning were only available for some leg joints (Mu and Ritzmann in J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191(11):1037–54, 2005) and thus had to be obtained using the methods that were applied for straight walking by Bender et al. (PloS one 5(10):1–15, 2010b). Once walking, inside turning, and outside turning were characterized, phase and amplitude changes for each joint of each leg were quantified. Apparent reflex reversals and joint activity changes were used to modify sensory coupling pathways between the CPG at each joint of the simulation. Oiled-plate experiments in simulation produced tarsus trajectories in stance similar to those seen in the animal. Simulations including forces that would be experienced if the insect was walking freely (i.e., weight support and friction) again produced similar results. These data were not considered during the design of the simulation, suggesting that the simulation captures some key underlying the principles of walking, turning, and transitioning in the cockroach. In addition, since the nervous system was modeled with realistic neuron models, biologically plausible reflex reversals are simulated, motivating future neurobiological research.

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

[2]  G. M. Hughes The Co-Ordination of Insect Movements I The Walking Movements of Insects , 1952 .

[3]  G. M. Hughes The Co-Ordination of Insect Movements , 1958 .

[4]  H. Cruse,et al.  Peripheral Influences on the Movement of the Legs in a Walking Insect Carausius Morosus , 1982 .

[5]  D. Graham,et al.  Behaviour and Motor Output of Stick Insects Walking on a Slippery Surface: I. Forward Walking , 1983 .

[6]  R. Calabrese,et al.  Slow oscillations of membrane potential in interneurons that control heartbeat in the medicinal leech , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  H. Cruse What mechanisms coordinate leg movement in walking arthropods? , 1990, Trends in Neurosciences.

[8]  R. Blickhan,et al.  Leg design in hexapedal runners. , 1991, The Journal of experimental biology.

[9]  H. Cruse,et al.  Movement of Joint Angles in the Legs of a Walking Insect, Carausius morosus , 1995 .

[10]  J. Schmitz,et al.  Rhythmic patterns in the thoracic nerve cord of the stick insect induced by pilocarpine , 1995, The Journal of experimental biology.

[11]  J. T. Watson,et al.  Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis: II. Fast running , 1997, Journal of Comparative Physiology A.

[12]  J. T. Watson,et al.  Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis : I. Slow running , 1997, Journal of Comparative Physiology A.

[13]  R. Full,et al.  Three-dimensional kinematics and limb kinetic energy of running cockroaches. , 1997, The Journal of experimental biology.

[14]  Thomas Kindermann,et al.  Walknet--a biologically inspired network to control six-legged walking , 1998, Neural Networks.

[15]  A. Büschges,et al.  Role of proprioceptive signals from an insect femur-tibia joint in patterning motoneuronal activity of an adjacent leg joint. , 1999, Journal of neurophysiology.

[16]  S. Zill,et al.  Active signaling of leg loading and unloading in the cockroach. , 1999, Journal of neurophysiology.

[17]  A K Tryba,et al.  Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. I. Kinematics and electromyograms. , 2000, Journal of neurophysiology.

[18]  T. Kindermann Behavior and Adaptability of a Six-Legged Walking System with Highly Distributed Control , 2001, Adapt. Behav..

[19]  U. Bässler,et al.  The role of sensory signals from the insect coxa-trochanteral joint in controlling motor activity of the femur-tibia joint. , 2001, Journal of neurophysiology.

[20]  Roy E. Ritzmann,et al.  Control of obstacle climbing in the cockroach, Blaberus discoidalis. I. Kinematics , 2002, Journal of Comparative Physiology A.

[21]  J. T. Watson,et al.  Control of climbing behavior in the cockroach, Blaberus discoidalis. II. Motor activities associated with joint movement , 2002, Journal of Comparative Physiology A.

[22]  Dirk Bucher,et al.  Interjoint coordination in the stick insect leg-control system: the role of positional signaling. , 2003, Journal of neurophysiology.

[23]  S. Zill,et al.  Walking on a ‘peg leg’: extensor muscle activities and sensory feedback after distal leg denervation in cockroaches , 2004, Journal of Comparative Physiology A.

[24]  A. Büschges,et al.  Dynamic simulation of insect walking. , 2004, Arthropod structure & development.

[25]  Michael A. Arbib,et al.  A mathematical analysis of the force-stiffness characteristics of muscles in control of a single joint system , 1992, Biological Cybernetics.

[26]  J. Schmitz,et al.  Identified nonspiking interneurons in leg reflexes and during walking in the stick insect , 1994, Journal of Comparative Physiology A.

[27]  J. Schmitz,et al.  Signals from load sensors underlie interjoint coordination during stepping movements of the stick insect leg. , 2004, Journal of neurophysiology.

[28]  R. Quinn,et al.  Convergent evolution and locomotion through complex terrain by insects, vertebrates and robots. , 2004, Arthropod structure & development.

[29]  A. Büschges,et al.  Synaptic drive contributing to rhythmic activation of motoneurons in the deafferented stick insect walking system , 2004, The European journal of neuroscience.

[30]  J. Schmitz,et al.  Load sensing and control of posture and locomotion. , 2004, Arthropod structure & development.

[31]  A. Büschges Sensory control and organization of neural networks mediating coordination of multisegmental organs for locomotion. , 2005, Journal of neurophysiology.

[32]  V. Dürr Context-dependent changes in strength and efficacy of leg coordination mechanisms , 2005, Journal of Experimental Biology.

[33]  V. Dürr,et al.  The behavioural transition from straight to curve walking: kinetics of leg movement parameters and the initiation of turning , 2005, Journal of Experimental Biology.

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

[35]  Volker Dürr,et al.  Insect walking is based on a decentralized architecture revealing a simple and robust controller , 2007, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[36]  A. Büschges,et al.  Tethered stick insect walking: A modified slippery surface setup with optomotor stimulation and electrical monitoring of tarsal contact , 2006, Journal of Neuroscience Methods.

[37]  A. J. Pollack,et al.  Multi-unit recording of antennal mechano-sensitive units in the central complex of the cockroach, Blaberus discoidalis , 2008, Journal of Comparative Physiology A.

[38]  Ansgar Büschges,et al.  Adaptive motor behavior in insects , 2007, Current Opinion in Neurobiology.

[39]  R. Ritzmann,et al.  Interaction between descending input and thoracic reflexes for joint coordination in cockroach: I. Descending influence on thoracic sensory reflexes , 2008, Journal of Comparative Physiology A.

[40]  J. Schmitz,et al.  Segment Specificity of Load Signal Processing Depends on Walking Direction in the Stick Insect Leg Muscle Control System , 2007, The Journal of Neuroscience.

[41]  Ilya A. Rybak,et al.  Control of oscillation periods and phase durations in half-center central pattern generators: a comparative mechanistic analysis , 2009, Journal of Computational Neuroscience.

[42]  Holk Cruse,et al.  No need for a body model: Positive velocity feedback for the control of an 18-DOF robot walker , 2008 .

[43]  Silvia Daun-Gruhn,et al.  An inter-segmental network model and its use in elucidating gait-switches in the stick insect , 2011, Journal of Computational Neuroscience.

[44]  Silvia Daun-Gruhn,et al.  A mathematical modeling study of inter-segmental coordination during stick insect walking , 2011, Journal of Computational Neuroscience.

[45]  Ying Zhu,et al.  AnimatLab: A 3D graphics environment for neuromechanical simulations , 2010, Journal of Neuroscience Methods.

[46]  Roy E. Ritzmann,et al.  Computer-Assisted 3D Kinematic Analysis of All Leg Joints in Walking Insects , 2010, PloS one.

[47]  A. Büschges,et al.  New Moves in Motor Control , 2011, Current Biology.

[48]  Roger D. Quinn,et al.  Descending commands to an insect leg controller network cause smooth behavioral transitions , 2011, 2011 IEEE/RSJ International Conference on Intelligent Robots and Systems.

[49]  J. Schmitz,et al.  Encoding of force increases and decreases by tibial campaniform sensilla in the stick insect, Carausius morosus , 2011, Journal of Comparative Physiology A.

[50]  Brian R. Tietz,et al.  Kinematic and behavioral evidence for a distinction between trotting and ambling gaits in the cockroach Blaberus discoidalis , 2011, Journal of Experimental Biology.

[51]  T I Tóth,et al.  A neuromechanical model explaining forward and backward stepping in the stick insect. , 2012, Journal of neurophysiology.

[52]  A. Büschges,et al.  Control of reflex reversal in stick insect walking: effects of intersegmental signals, changes in direction, and optomotor-induced turning. , 2012, Journal of neurophysiology.

[53]  Thierry Hoinville,et al.  A hexapod walker using a heterarchical architecture for action selection , 2013, Front. Comput. Neurosci..

[54]  Panayiota Poirazi,et al.  Computational modeling of the effects of amyloid-beta on release probability at hippocampal synapses , 2013, Front. Comput. Neurosci..

[55]  Thierry Hoinville,et al.  Walknet, a bio-inspired controller for hexapod walking , 2013, Biological Cybernetics.

[56]  R. Ritzmann,et al.  Neural activity in the central complex of the cockroach brain is linked to turning behaviors , 2013, Journal of Experimental Biology.