Neural Mechanisms Underlying Direction-Selective Avoidance Behavior

Avoiding looming objects (possible predators) is essential for animals'survival. This article presents a neural network model to account for the detection of and response to a looming stimulus. The generation of an appropriate response includes five tasks: detection of a looming stimulus, localization of the stimulus position, computation of the direction of the stimulus movement, determination of escape direction, and selection of a proper motor action. The detection of a looming stimulus is achieved based on the expansion of the retinal image and depth information. The spatial location of the stimulus is encoded by a population of neurons. The direction of the looming stimulus is computed by monitoring the shift of the peak of neuronal activity in this population. The signal encoding the stimulus location is gated by the direction- selective neurons onto a motor heading map, which specifies the escape direction. The selection of a proper action is achieved through competition among different groups of motor neurons. The model is based on the analysis of predator-avoidance in frog and toad but leads to a comparative analysis of mammalian visual systems.

[1]  D. Ingle 4 – Spatial Vision in Anurans , 1976 .

[2]  C. Koch,et al.  The analysis of visual motion: from computational theory to neuronal mechanisms. , 1986, Annual review of neuroscience.

[3]  A Cobas,et al.  Prey-catching and predator-avoidance in frog and toad: defining the schemas. , 1992, Journal of theoretical biology.

[4]  D. Ingle,et al.  Visually Elicited Evasive Behavior in FrogsGiving memory research an ethological context , 1990 .

[5]  David Ingle Control of frog evasive direction: triggering and biasing systems , 1991 .

[6]  Donald H. House Depth Perception in Frogs and Toads: A Study in Neural Computing , 1989 .

[7]  P. Grobstein,et al.  Tectal connectivity in the frog Rana pipiens: Tectotegmental projections and a general analysis of topographic organization , 1990, The Journal of comparative neurology.

[8]  J T Todd,et al.  Visual information about moving objects. , 1981, Journal of experimental psychology. Human perception and performance.

[9]  E. Knudsen,et al.  Horizontal and vertical components of head movement are controlled by distinct neural circuits in the barn owl , 1990, Nature.

[10]  J. Tresilian,et al.  Empirical and theoretical issues in the perception of time to contact. , 1991, Journal of experimental psychology. Human perception and performance.

[11]  M. Cynader,et al.  Neurones in cat parastriate cortex sensitive to the direction of motion in three‐dimensional space , 1978, The Journal of physiology.

[12]  J. Ewert The neural basis of visually guided behavior. , 1974, Scientific American.

[13]  V. Henn,et al.  Vertical eye movement related unit activity in the rostral mesencephalic reticular formation of the alert monkey , 1977, Brain Research.

[14]  W von Seelen,et al.  [Neurobiology and system theory of a visual pattern recognition mechanism in the toad]. , 1973, Kybernetik.

[15]  Jan J. Koenderink,et al.  Local structure of movement parallax of the plane , 1976 .

[16]  B. Frost,et al.  Time to collision is signalled by neurons in the nucleus rotundus of pigeons , 1992, Nature.

[17]  W Reichardt,et al.  Functional structure of a mechanism of perception of optical movement , 1958 .

[18]  D. Ingle Brain Mechanisms of Visual Localization by Frogs and Toads , 1983 .

[19]  J F Soechting,et al.  Parcellation of sensorimotor transformations for arm movements , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  J. C. Coggshall,et al.  The Landing Response and Visual Processing in the Milkweed Bug, Oncopeltus Fasciatus , 1972 .

[21]  H Spekreijse,et al.  Responses to directional stimuli in retinal preganglionic units , 1970, The Journal of physiology.

[22]  H. Barlow,et al.  Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit , 1964, The Journal of physiology.

[23]  Nicholas G. Hatsopoulos,et al.  Visual navigation with a neural network , 1991, Neural Networks.

[24]  Margaret E. Sereno,et al.  Learning to See Rotation and Dilation with a Hebb Rule , 1990, NIPS.

[25]  J. Ewert Neuroethology of releasing mechanisms: Prey-catching in toads , 1987, Behavioral and Brain Sciences.

[26]  H B BARLOW,et al.  Action potentials from the frog's retina , 1953, The Journal of physiology.

[27]  S Hemilä,et al.  Directional selectivity and colour coding in the frog retina. , 1978, Medical biology.

[28]  David N. Lee,et al.  A Theory of Visual Control of Braking Based on Information about Time-to-Collision , 1976, Perception.

[29]  Ken Nakayama,et al.  Biological image motion processing: A review , 1985, Vision Research.

[30]  K. Tanaka,et al.  Underlying mechanisms of the response specificity of expansion/contraction and rotation cells in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[31]  J. Ewert Tectal Mechanisms That Underlie Prey-Catching and Avoidance Behaviors in Toads , 1984 .

[32]  M. Arbib,et al.  A neural model of interactions subserving prey-predator discrimination and size preference in anuran amphibia. , 1985, Journal of theoretical biology.

[33]  J. Dowling,et al.  Physiology and Morphology of the Retina , 1976 .

[34]  S. Watanabe,et al.  Synaptic mechanisms of directional selectivity in ganglion cells of frog retina as revealed by intracellular recordings. , 1984, The Japanese journal of physiology.

[35]  U Grüsser-Cornehls,et al.  Velocity sensitivity and directional selectivity of frog retinal ganglion cells depend on chromaticity of moving stimuli. , 1985, Brain, behavior and evolution.

[36]  B. C. Motter,et al.  The functional properties of the light-sensitive neurons of the posterior parietal cortex studied in waking monkeys: foveal sparing and opponent vector organization , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  O. Grüsser,et al.  Neurophysiology of the Anuran Visual System , 1976 .

[38]  W. Reichardt Movement perception in insects , 1969 .

[39]  W. Schiff PERCEPTION OF IMPENDING COLLISION: A STUDY OF VISUALLY DIRECTED AVOIDANT BEHAVIOR. , 1965, Psychological monographs.

[40]  Keiji Tanaka,et al.  Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  Paul Grobstein,et al.  Organization in the Sensorimotor Interface: A Case Study with Increased Resolution , 1989 .

[42]  D. Regan,et al.  Evidence for the existence of neural mechanisms selectively sensitive to the direction of movement in space , 1973, The Journal of physiology.

[43]  O. Grüsser,et al.  Neuronal Mechanisms of Visual Movement Perception and Some Psychophysical and Behavioral Correlations , 1973 .

[44]  G. Wasilkowski,et al.  Computing optical flow , 1989, [1989] Proceedings. Workshop on Visual Motion.

[45]  J. Ewert,et al.  Quantitative Analyse Der Reiz-Reaktionsbeziehungen Bei Visuellem Auslösen Des Fluchtverhaltens Der Wechselkröte (Bufo Viridis Laur.) , 1969 .

[46]  D. Ingle,et al.  Receptive field changes produced in frog thalamic units by lesions of the optic tectum. , 1973, Brain research.

[47]  Donald H. House,et al.  Depth Perception in Frogs and Toads , 1989 .

[48]  J. F. Soechting,et al.  Early stages in a sensorimotor transformation , 1992, Behavioral and Brain Sciences.

[49]  T. Freeman,et al.  Human sensitivity to expanding and rotating motion: effects of complementary masking and directional structure , 1992, Vision Research.

[50]  L E Mays,et al.  Signal transformations required for the generation of saccadic eye movements. , 1990, Annual review of neuroscience.

[51]  Lee Dn,et al.  The optic flow field: the foundation of vision. , 1980 .

[52]  W Schiff,et al.  Information Used in Judging Impending Collision , 1979, Perception.

[53]  Christof Koch,et al.  Computing Optical Flow in the Primate Visual System , 1989, Neural Computation.

[54]  H. K. Hartline,et al.  THE RECEPTIVE FIELDS OF OPTIC NERVE FIBERS , 1940 .

[55]  B Cohen,et al.  Horizontal saccades and the central mesencephalic reticular formation. , 1986, Progress in brain research.