The cricket cercal system implements delay-line processing.

The cercal sensory system of crickets mediates sensitivity to low-amplitude air currents. The sense organ for this system is a pair of antenna-like abdominal appendages called cerci, each of which is about 1 cm long in normal adult crickets. Although this system has been used extensively as a model system for studying the mechanisms underlying neural coding at the cellular and system levels, no previous studies have considered the functional significance of the physical dimensions of cerci. We show that the differential conduction characteristics of the receptor array in Acheta domesticus crickets are of substantial significance. All filiform sensory afferent axons we examined had the same propagation speeds to within a small variance, resulting in a significant and systematic differential propagation time for spikes from sensory receptors at different locations along the structure. Thus the sensory structures operate as delay lines. The delay-line structure supports neural computations in many of the projecting cercal interneurons (INs) that yield substantial differential sensitivity to the direction and velocity of naturalistic stimuli. Several INs show delay-line-derived sensitivities that are equivalent, in an engineering sense, to "notch filtering," through which background noise is selectively eliminated by the delay-line-based processing.

[1]  K. M. Chapman,et al.  Conduction Velocities and Their Temperature Coefficients in Sensory Nerve Fibres of Cockroach Legs , 1967 .

[2]  Francesco Lacquaniti,et al.  Kinematics in Newly Walking Toddlers Does Not Depend Upon Postural Stability , 2005 .

[3]  Jeffrey M. Camhi,et al.  The escape behavior of the cockroachPeriplaneta americana , 2004, Journal of comparative physiology.

[4]  Jürgen Tautz,et al.  Caterpillars detect flying wasps by hairs sensitive to airborne vibration , 1978, Behavioral Ecology and Sociobiology.

[5]  G. Jacobs,et al.  Direction sensitivity of the filiform hair population of the cricket cereal system , 1995, Journal of Comparative Physiology A.

[6]  R. Batra,et al.  Axons from Anteroventral Cochlear Nucleus that Terminate in Medial Superior Olive of Cat: Observations Related to Delay Lines , 1999, The Journal of Neuroscience.

[7]  W. Heetderks,et al.  Partition of gross peripheral nerve activity into single unit responses by correlation techniques. , 1975, Science.

[8]  Ulrich G. Hofmann,et al.  Test of spike-sorting algorithms on the basis of simulated network data , 2002, Neurocomputing.

[9]  F. Theunissen,et al.  Extraction of Sensory Parameters from a Neural Map by Primary Sensory Interneurons , 2000, The Journal of Neuroscience.

[10]  Thomas Steinmann,et al.  The Aerodynamic Signature of Running Spiders , 2008, PloS one.

[11]  John Zachary Young,et al.  Fused Neurons and Synaptic Contacts in the Giant Nerve Fibres of Cephalopods , 1939 .

[12]  Shigeru Shinomoto,et al.  New classification scheme of cortical sites with the neuronal spiking characteristics , 2002, Neural Networks.

[13]  Jeffrey M. Camhi,et al.  The escape behavior of the cockroachPeriplaneta americana , 1978, Journal of comparative physiology.

[14]  N Suga,et al.  Long delay lines for ranging are created by inhibition in the inferior colliculus of the mustached bat. , 1995, Journal of neurophysiology.

[15]  George Zouridakis,et al.  Identification of reliable spike templates in multi-unit extracellular recordings using fuzzy clustering , 2000, Comput. Methods Programs Biomed..

[16]  L. Liu,et al.  A method of neuronal spike train study based on autoregressive analysis , 1989, Biological Cybernetics.

[17]  K. Dumpert,et al.  Cricket combined mechanoreceptors and kicking response , 2004, Journal of comparative physiology.

[18]  C. M. Comer,et al.  Multisensory control of escape in the cockroach Penplaneta americana , 2004, Journal of Comparative Physiology A.

[19]  Wilfrid Rall,et al.  Theoretical significance of dendritic trees for neuronal input-output relations , 1964 .

[20]  Yoshio Sakurai,et al.  Automatic sorting for multi-neuronal activity recorded with tetrodes in the presence of overlapping spikes. , 2003, Journal of neurophysiology.

[21]  W. Gnatzy,et al.  Digger wasp against crickets , 1986, Naturwissenschaften.

[22]  Steven M. Bierer,et al.  Multi-channel spike detection and sorting using an array processing technique , 1999, Neurocomputing.

[23]  F. Theunissen,et al.  Functional organization of a neural map in the cricket cercal sensory system , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  G A Jacobs,et al.  Segmental origins of the cricket giant interneuron system , 1987, The Journal of comparative neurology.

[25]  斉藤 勲 Long delay lines for ranging are created by inhibition in the inferior colliculus of the mustached bat , 1997 .

[26]  R. Llinás,et al.  Uniform olivocerebellar conduction time underlies Purkinje cell complex spike synchronicity in the rat cerebellum. , 1993, The Journal of physiology.

[27]  T. Steinmann,et al.  Spider's attack versus cricket's escape: velocity modes determine success , 2006, Animal Behaviour.

[28]  Richard Julius Pumphrey,et al.  Synaptic transmission of nervous impulses through the last abdominal ganglion of the cockroach , 1937 .

[29]  R. Segev,et al.  A method for spike sorting and detection based on wavelet packets and Shannon's mutual information , 2002, Journal of Neuroscience Methods.

[30]  J. Letelier,et al.  Spike sorting based on discrete wavelet transform coefficients , 2000, Journal of Neuroscience Methods.

[31]  T. Sejnowski,et al.  Independent component analysis at the neural cocktail party , 2001, Trends in Neurosciences.

[32]  John P. Miller,et al.  Phased array processing for spike discrimination , 2005, Neurocomputing.

[33]  Jeffrey M. Camhi,et al.  THE ESCAPE BEHAVIOR OF THE COCKROACH PERIPLANETA AMERICANA. II. DETECTION OF NATURAL PREDATORS BY AIR DISPLACEMENT , 1978 .

[34]  Brian Everitt,et al.  Cluster analysis , 1974 .

[35]  B.D. Van Veen,et al.  Beamforming: a versatile approach to spatial filtering , 1988, IEEE ASSP Magazine.

[36]  Bruce C. Wheeler,et al.  A Comparison of Techniques for Classification of Multiple Neural Signals , 1982, IEEE Transactions on Biomedical Engineering.

[37]  A.F. Atiya,et al.  Recognition of multiunit neural signals , 1992, IEEE Transactions on Biomedical Engineering.

[38]  Dinh-Tuan Pham,et al.  Blind separation of instantaneous mixtures of nonstationary sources , 2001, IEEE Trans. Signal Process..

[39]  J. Okada,et al.  Multineuronal spike classification based on multisite electrode recording, whole-waveform analysis, and hierarchical clustering , 1999, IEEE Transactions on Biomedical Engineering.

[40]  J. Bacon,et al.  Receptive fields of cricket giant interneurones are related to their dendritic structure. , 1984, The Journal of physiology.

[41]  Karim G. Oweiss,et al.  Noise reduction in multichannel neural recordings using a new array wavelet denoising algorithm , 2001, Neurocomputing.

[42]  James N. Campbell,et al.  Coupling between unmyelinated peripheral nerve fibers does not involve sympathetic efferent fibers , 1987, Brain Research.

[43]  Daniel K. Hartline,et al.  Separation of multi-unit nerve impulse trains by a multi-channel linear filter algorithm , 1975, Brain Research.

[44]  James N. Campbell,et al.  Coupling of action potential activity between unmyelinated fibers in the peripheral nerve of monkey , 1985 .

[45]  M. Dambach,et al.  Response of the cercus-to-giant interneuron system in crickets to species-specific song , 1981, Journal of comparative physiology.

[46]  J. Camhi,et al.  The wind-evoked escape behavior of the cricket Gryllus bimaculatus: integration of behavioral elements , 1995, The Journal of experimental biology.

[47]  M. O'Shea,et al.  Pentapeptide (proctolin) associated with an identified neuron. , 1981, Science.

[48]  Jérôme Casas,et al.  Hair canopy of cricket sensory system tuned to predator signals. , 2006, Journal of theoretical biology.

[49]  Jérôme Casas,et al.  Variability in Sensory Ecology: Expanding the Bridge Between Physiology and Evolutionary Biology , 2009, The Quarterly Review of Biology.

[50]  J Palka,et al.  The cerci and abdominal giant fibres of the house cricket, Acheta domesticus. I. Anatomy and physiology of normal adults , 1974, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[51]  Jan W. H. Schnupp,et al.  On hearing with more than one ear: lessons from evolution , 2009, Nature Neuroscience.

[52]  Edward M. Schmidt,et al.  Computer separation of multi-unit neuroelectric data: a review , 1984, Journal of Neuroscience Methods.

[53]  M. Hörner,et al.  A comparison of spontaneous and wind-evoked running modes in crickets and cockroaches , 1994 .

[54]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

[55]  D. Brillinger The maximum likelihood approach to the identification of neuronal firing systems , 2006, Annals of Biomedical Engineering.

[56]  R. Chandra,et al.  Detection, classification, and superposition resolution of action potentials in multiunit single-channel recordings by an on-line real-time neural network , 1997, IEEE Transactions on Biomedical Engineering.

[57]  William J. Williams,et al.  Transfer Characteristics of Dispersive Nerve Bundles , 1972, IEEE Trans. Syst. Man Cybern..

[58]  Gwen A. Jacobs,et al.  Predicting Emergent Properties of Neuronal Ensembles Using a Database of Individual Neurons , 2002 .

[59]  B. Wheeler,et al.  A flexible perforated microelectrode array for extended neural recordings , 1992, IEEE Transactions on Biomedical Engineering.

[60]  John Palka,et al.  The cercus-to-giant interneuron system of crickets , 2004, Journal of comparative physiology.

[61]  Hans-Georg Heinzel,et al.  Travelling air vortex rings as potential communication signals in a cricket , 2004, Journal of Comparative Physiology A.

[62]  Kate L. Christison-Lagay,et al.  A mechanism for neuronal coincidence revealed in the crayfish antennule , 2008, Proceedings of the National Academy of Sciences.

[63]  C E Carr,et al.  Processing of temporal information in the brain. , 1993, Annual review of neuroscience.

[64]  A. Spence,et al.  A micromachined silicon multielectrode for multiunit recording , 2003, Journal of Neuroscience Methods.

[65]  G. Jacobs,et al.  Neural Mapping of Direction and Frequency in the Cricket Cercal Sensory System , 1999, The Journal of Neuroscience.

[66]  Z. Aldworth,et al.  Computational mechanisms of mechanosensory processing in the cricket , 2008, Journal of Experimental Biology.

[67]  M. Konishi,et al.  Axonal delay lines for time measurement in the owl's brainstem. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[68]  W. Gnatzy,et al.  Digger wasp against crickets. II. An airborne signal produced by a running predator , 1990, Journal of Comparative Physiology A.

[69]  C. Carr,et al.  A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  C. M. Comer,et al.  Multisensory control of escape in the cockroach Periplaneta americana , 2004, Journal of Comparative Physiology A.

[71]  Tateo Shimozawa,et al.  The aerodynamics and sensory physiology of range fractionation in the cereal filiform sensilla of the cricketGryllus bimaculatus , 1984, Journal of Comparative Physiology A.