Computation of object approach by a system of visual motion-sensitive neurons in the crab Neohelice.

Similar to most visual animals, crabs perform proper avoidance responses to objects directly approaching them. The monostratified lobula giant neurons of type 1 (MLG1) of crabs constitute an ensemble of 14-16 bilateral pairs of motion-detecting neurons projecting from the lobula (third optic neuropile) to the midbrain, with receptive fields that are distributed over the extensive visual field of the animal's eye. Considering the crab Neohelice (previously Chasmagnathus) granulata, here we describe the response of these neurons to looming stimuli that simulate objects approaching the animal on a collision course. We found that the peak firing time of MLG1 acts as an angular threshold detector signaling, with a delay of δ = 35 ms, the time at which an object reaches a fixed angular threshold of 49°. Using in vivo intracellular recordings, we detected the existence of excitatory and inhibitory synaptic currents that shape the neural response. Other functional features identified in the MLG1 neurons were phasic responses at the beginning of the approach, a relation between the stimulus angular velocity and the excitation delay, and a mapping between membrane potential and firing frequency. Using this information, we propose a biophysical model of the mechanisms that regulate the encoding of looming stimuli. Furthermore, we found that the parameter encoded by the MLG1 firing frequency during the approach is the stimulus angular velocity. The proposed model fits the experimental results and predicts the neural response to a qualitatively different stimulus. Based on these and previous results, we propose that the MLG1 neuron system acts as a directional coding system for collision avoidance.

[1]  Michael H Dickinson,et al.  Collision-avoidance and landing responses are mediated by separate pathways in the fruit fly, Drosophila melanogaster. , 2002, The Journal of experimental biology.

[2]  F. Claire Rind,et al.  Non-directional, movement sensitive neurones of the locust optic lobe , 1987, Journal of Comparative Physiology A.

[3]  F Gabbiani,et al.  Collision-avoidance behaviors of minimally restrained flying locusts to looming stimuli , 2013, Journal of Experimental Biology.

[4]  Terrence J. Sejnowski,et al.  An Efficient Method for Computing Synaptic Conductances Based on a Kinetic Model of Receptor Binding , 1994, Neural Computation.

[5]  N. Strausfeld,et al.  Organization of optic lobes that support motion detection in a semiterrestrial crab , 2005, The Journal of comparative neurology.

[6]  D. Tomsic,et al.  How visual space maps in the optic neuropils of a crab , 2011, The Journal of comparative neurology.

[7]  Jan M. Hemmi,et al.  Predator avoidance in fiddler crabs: 2. The visual cues , 2005, Animal Behaviour.

[8]  F. Claire Rind,et al.  Motor activity and trajectory control during escape jumping in the locust Locusta migratoria , 2005, Journal of Comparative Physiology A.

[9]  Bilateral flight muscle activity predicts wing kinematics and 3-dimensional body orientation of locusts responding to looming objects , 2013, Journal of Experimental Biology.

[10]  Damián E. Oliva,et al.  Characterization of lobula giant neurons responsive to visual stimuli that elicit escape behaviors in the crab Chasmagnathus. , 2007, Journal of neurophysiology.

[11]  N. Strausfeld The evolution of crustacean and insect optic lobes and the origins of chiasmata , 2005 .

[12]  John R Gray,et al.  Habituated visual neurons in locusts remain sensitive to novel looming objects , 2005, Journal of Experimental Biology.

[13]  Damián Oliva,et al.  Collision Avoidance Models, Visually Guided , 2014, Encyclopedia of Computational Neuroscience.

[14]  D. Tomsic,et al.  Binocular visual integration in the crustacean nervous system , 2004, Journal of Comparative Physiology A.

[15]  Roger C. Hardie,et al.  Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly , 1978, Journal of comparative physiology.

[16]  G. Schlotterer Response of the locust descending movement detector neuron to rapidly approaching and withdrawing visual stimuli , 1977 .

[17]  P. Simmons,et al.  Seeing what is coming: building collision-sensitive neurones , 1999, Trends in Neurosciences.

[18]  D. Tomsic,et al.  Physiology and morphology of visual movement detector neurons in a crab (Decapoda: Brachyura) , 2002, Journal of Comparative Physiology A.

[19]  M. Land,et al.  The visual control of behaviour in fiddler crabs , 1995, Journal of Comparative Physiology A.

[20]  H. Krapp,et al.  Spatial distribution of inputs and local receptive field properties of a wide-field, looming sensitive neuron. , 2005, Journal of neurophysiology.

[21]  D. Tomsic,et al.  Neuronal correlates of the visually elicited escape response of the crab Chasmagnathus upon seasonal variations, stimuli changes and perceptual alterations , 2008, Journal of Comparative Physiology A.

[22]  G. Laurent,et al.  Computation of Object Approach by a Wide-Field, Motion-Sensitive Neuron , 1999, The Journal of Neuroscience.

[23]  R. Glantz Habituation of the motion detectors of the crayfish optic nerve: their relationship to the visually evoked defense reflex. , 1974, Journal of neurobiology.

[24]  Damián E. Oliva Mecanismos de detección visual y evitación de colisiones en un nuevo modelo experimental, el cangrejo Chasmagnathus granulatus , 2010 .

[25]  Jan M. Hemmi,et al.  Predator avoidance in fiddler crabs: 1. Escape decisions in relation to the risk of predation , 2005, Animal Behaviour.

[26]  P. Simmons,et al.  Gliding behaviour elicited by lateral looming stimuli in flying locusts , 2004, Journal of Comparative Physiology A.

[27]  N. Strausfeld,et al.  Neural organization of first optic neuropils in the littoral crab Hemigrapsus oregonensis and the semiterrestrial species Chasmagnathus granulatus , 2009, The Journal of comparative neurology.

[28]  P. Simmons,et al.  Orthopteran DCMD neuron: a reevaluation of responses to moving objects. I. Selective responses to approaching objects. , 1992, Journal of neurophysiology.

[29]  F. Gabbiani,et al.  A novel neuronal pathway for visually guided escape in Drosophila melanogaster. , 2009, Journal of neurophysiology.

[30]  Damián Oliva,et al.  Visuo-motor transformations involved in the escape response to looming stimuli in the crab Neohelice (=Chasmagnathus) granulata , 2012, Journal of Experimental Biology.

[31]  Y. Toh,et al.  Responses of descending neurons to looming stimuli in the praying mantis Tenodera aridifolia , 2009, Journal of Comparative Physiology A.

[32]  Larry Wasserman,et al.  All of Statistics: A Concise Course in Statistical Inference , 2004 .

[33]  F. Gabbiani,et al.  Logarithmic Compression of Sensory Signals within the Dendritic Tree of a Collision-Sensitive Neuron , 2012, The Journal of Neuroscience.

[34]  Daniel Tomsic,et al.  Brain Modularity in Arthropods: Individual Neurons That Support “What” But Not “Where” Memories , 2011, The Journal of Neuroscience.

[35]  F. Dodge,et al.  Prediction of maximum allowable retinal slip speed in the fiddler crab, Uca pugilator. , 1997, The Biological bulletin.

[36]  Hans-Ortwin Nalbach Visually Elicited Escape in Crabs , 1990 .

[37]  F. Rind,et al.  Neural network based on the input organization of an identified neuron signaling impending collision. , 1996, Journal of neurophysiology.

[38]  D. Tomsic,et al.  Regionalization in the eye of the grapsid crab Neohelice granulata (=Chasmagnathus granulatus): variation of resolution and facet diameters , 2012, Journal of Comparative Physiology A.

[39]  Fabrizio Gabbiani,et al.  Collision detection as a model for sensory-motor integration. , 2011, Annual review of neuroscience.

[40]  M. O'Shea,et al.  Protection from habituation by lateral inhibition , 1975, Nature.

[41]  D. Tomsic,et al.  Escape behavior and neuronal responses to looming stimuli in the crab Chasmagnathus granulatus (Decapoda: Grapsidae) , 2007, Journal of Experimental Biology.

[42]  R. Robertson,et al.  A pair of motion-sensitive neurons in the locust encode approaches of a looming object , 2010, Journal of Comparative Physiology A.

[43]  M. Srinivasan,et al.  Visual motor computations in insects. , 2004, Annual review of neuroscience.

[44]  O. Iribarne,et al.  Predation on the southwestern Atlantic fiddler crab (Uca uruguayensis) by migratory shorebirds (pluvialis dominica, P. squatarola, arenaria interpres, and numenius phaeopus) , 1999 .

[45]  F. Gabbiani,et al.  Relationship between the Phases of Sensory and Motor Activity during a Looming-Evoked Multistage Escape Behavior , 2007, The Journal of Neuroscience.

[46]  S. Peron,et al.  Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron , 2009, Nature Neuroscience.

[47]  G. Laurent,et al.  Invariance of Angular Threshold Computation in a Wide-Field Looming-Sensitive Neuron , 2001, The Journal of Neuroscience.

[48]  C. Koch,et al.  Multiplicative computation in a visual neuron sensitive to looming , 2002, Nature.

[49]  D. Tomsic,et al.  The neuroethology of escape in crabs: from sensory ecology to neurons and back , 2012, Current Opinion in Neurobiology.

[50]  Alexander Borst,et al.  Spatiotemporal Response Properties of Optic-Flow Processing Neurons , 2010, Neuron.

[51]  Y. Toh,et al.  Response Properties of Visual Interneurons to Motion Stimuli in the Praying Mantis, Tenodera aridifolia , 2003, Zoological science.

[52]  J. Herberholz,et al.  Decision Making and Behavioral Choice during Predator Avoidance , 2012, Front. Neurosci..

[53]  G. Card,et al.  Escape behaviors in insects , 2012, Current Opinion in Neurobiology.

[54]  F. Gabbiani,et al.  Report Synchronized Neural Input Shapes Stimulus Selectivity in a Collision-detecting Neuron , 2022 .

[55]  R. Glantz Defense reflex and motion detector responsiveness to approaching targets: The motion detector trigger to the defense reflex pathway , 1974, Journal of comparative physiology.

[56]  D. Tomsic,et al.  Identification of Individual Neurons Reflecting Short- and Long-Term Visual Memory in an Arthropodo , 2003, The Journal of Neuroscience.

[57]  M. O'Shea,et al.  NEURONAL BASIS OF A SENSORY ANALYSER , THE ACRID ID MOVEMENT DETECTOR SYSTEM , 2005 .

[58]  Hang Zhang,et al.  Ubiquitous Log Odds: A Common Representation of Probability and Frequency Distortion in Perception, Action, and Cognition , 2012, Front. Neurosci..