Chapter 2 The biological bases of time-to-collision computation

Abstract We begin the chapter by arguing that there may be several neural mechanisms that have evolved for computing time-to-collision (TTC) information as a way of controlling different classes of action. We then focus on single unit mechanisms responsible for processing the impending collision of a moving object towards a stationary observer. After discussing TTC processing in the invertebrate visual system, we describe our own work involving neurons in the pigeon nucleus rotundus that respond exclusively to visual information relating to objects that are approaching on a direct collision course, but not to visual information simulating observer's movement towards those same stationary objects. Based on the recorded neuronal responses to various manipulations of the stimuli, we classified these looming sensitive neurons into three different types of looming detectors based on the temporal differences in neuronal response relative to the moment of collision. We also described quantitative models for these looming detectors as a way of explaining their physiological response properties.

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

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

[3]  N. Strausfeld,et al.  Organization and significance of neurons that detect change of visual depth in the hawk moth Manduca sexta , 2000, The Journal of comparative neurology.

[4]  W. J. Heitler,et al.  Triggering of locust jump by multimodal inhibitory interneurons. , 1980, Journal of neurophysiology.

[5]  M. Goodale,et al.  The role of the predorsal bundle in head and body movements elicited by electrical stimulation of the superior colliculus in the Mongolian gerbil , 2004, Experimental Brain Research.

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

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

[8]  Rind,et al.  The locust DCMD, a movement-detecting neurone tightly tuned to collision trajectories , 1997, The Journal of experimental biology.

[9]  M. Goodale,et al.  A functional analysis of the collicular output pathways: a dissociation of deficits following lesions of the dorsal tegmental decussation and the ipsilateral collicular efferent bundle in the Mongolian gerbil , 2004, Experimental Brain Research.

[10]  H. Wagner Flow-field variables trigger landing in flies , 1982, Nature.

[11]  Peter Redgrave,et al.  Gnawing and changes in reactivity produced by microinjections of picrotoxin into the superior colliculus of rats , 2004, Psychopharmacology.

[12]  E. Reed The Ecological Approach to Visual Perception , 1989 .

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

[14]  Peter Redgrave,et al.  Cardiovascular and respiratory changes elicited by stimulation of rat superior colliculus , 1988, Brain Research Bulletin.

[15]  R. M. Robertson,et al.  Retinal image size triggers obstacle avoidance in flying locusts , 1993, Naturwissenschaften.

[16]  H. Vanegas,et al.  Comparative neurology of the optic tectum , 1984 .

[17]  Albert Yonas,et al.  The Development of Sensitivity of Kenetic, Binocular and Pictorial Depth Information in Human Infants , 1985 .

[18]  R. Fishman,et al.  Studies of Visual Depth Perception: II. Avoidance Reaction as an Indicator Response in Chicks , 1961 .

[19]  W. Hodos,et al.  Intensity, color, and pattern discrimination deficits after lesions of the core and belt regions of the ectostriatum , 1989, Visual Neuroscience.

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

[21]  M. Goodale,et al.  A mammalian model of optic-flow utilization in the control of locomotion , 2004, Experimental Brain Research.

[22]  Paul A. Braren,et al.  How We Avoid Collisions With Stationary and Moving Obstacles , 2004 .

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

[24]  P Redgrave,et al.  Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  D. Ingle,et al.  Action-Oriented Approaches to Visuo-Spatial Brain Functions , 1985 .

[26]  R. Olberg,et al.  Prey pursuit and interception in dragonflies , 2000, Journal of Comparative Physiology A.

[27]  Lawrence M. Dill,et al.  The escape response of the zebra danio (Brachydanio rerio) I. The stimulus for escape , 1974 .

[28]  Christof Koch,et al.  Multiplicative computation by a looming-sensitive neuron , 2002, Proceedings of the Second Joint 24th Annual Conference and the Annual Fall Meeting of the Biomedical Engineering Society] [Engineering in Medicine and Biology.

[29]  B. Frost,et al.  Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons , 1998, Nature Neuroscience.

[30]  P. Cavanagh,et al.  Deep tectal cells in pigeons respond to kinematograms , 1988, Journal of Comparative Physiology A.

[31]  R. Robertson,et al.  Collision avoidance of flying locusts: steering torques and behaviour , 1993 .

[32]  Peter J. Simmons,et al.  Connexions between a movement-detecting visual interneurone and flight motoneurones of a locust. , 1980 .

[33]  W. Hodos Color Discrimination Deficits After Lesions of the Nucleus Rotundus in Pigeons , 1969 .

[34]  M Konishi,et al.  Auditory Spatial Receptive Fields Created by Multiplication , 2001, Science.

[35]  E. Tronick,et al.  Approach response of domestic chicks to an optical display. , 1967, Journal of comparative and physiological psychology.

[36]  David N. Lee,et al.  Plummeting gannets: a paradigm of ecological optics , 1981, Nature.

[37]  David N. Lee,et al.  VISUAL CONTROL OF VELOCITY OF APPROACH BY PIGEONS WHEN LANDING , 1993 .

[38]  James A. Caviness,et al.  Persistent Fear Responses in Rhesus Monkeys to the Optical Stimulus of "Looming" , 1962, Science.

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

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

[41]  P. L. Scilley,et al.  Moving background patterns reveal double-opponency of directionally specific pigeon tectal neurons , 2004, Experimental Brain Research.

[42]  G. Schneider,et al.  Behavior evoked by electrical stimulation of the hamster superior colliculus , 2004, Experimental Brain Research.

[43]  F C Rind,et al.  Orthopteran DCMD neuron: a reevaluation of responses to moving objects. II. Critical cues for detecting approaching objects. , 1992, Journal of neurophysiology.

[44]  J. Gibson The Ecological Approach to Visual Perception , 1979 .

[45]  M. Burrows,et al.  Connections between descending visual interneurons and metathoracic motoneurons in the locust , 1973, Journal of comparative physiology.

[46]  Hong-jin Sun,et al.  Contextual influences on the directional responses of tectal cells in pigeons , 2002, Visual Neuroscience.

[47]  C. Jarvis Visual discrimination and spatial localization deficits after lesions of the tectofugal pathway in pigeons. , 1974, Brain, behavior and evolution.

[48]  W. N. Hayes,et al.  Visual alarm reactions in turtles. , 1967, Animal behaviour.

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

[50]  D. Ingle,et al.  Brain mechanisms and spatial vision , 1985 .

[51]  B. J. Frost,et al.  Moving background patterns alter directionally specific responses of pigeon tectal neurons , 1978, Brain Research.

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

[53]  K. Nakayama,et al.  Single visual neurons code opposing motion independent of direction. , 1983, Science.

[54]  H. Karten,et al.  Brightness and pattern discrimination deficits in the pigeon after lesions of nucleus rotundus , 2004, Experimental Brain Research.

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

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

[57]  W. Ball,et al.  Infant Responses to Impending Collision: Optical and Real , 1971, Science.

[58]  Svetha Venkatesh,et al.  From Living Eyes to Seeing Machines , 1997 .

[59]  G. Laurent,et al.  Elementary Computation of Object Approach by a Wide-Field Visual Neuron , 1995, Science.

[60]  E. M. Lee,et al.  Taming of wild Rattus norvegicus by lesions of the mesencephalic central gray , 1981 .

[61]  W. Hodos,et al.  Intensity difference thresholds in pigeons after lesions of the tectofugal and thalamofugal visual pathways. , 1974, Journal of comparative and physiological psychology.

[62]  P. Dean,et al.  Responses resembling defensive behaviour produced by microinjection of glutamate into superior colliculus of rats , 1988, Neuroscience.

[63]  T. Bower,et al.  Infant responses to approaching objects: An indicator of response to distal variables , 1971 .