Tectal neurons signal impending collision of looming objects in the pigeon

Although the optic tectum in non‐mammals and its mammalian homolog, the superior colliculus, are involved in avoidance behaviors, whether and how tectal neurons respond to an object approaching on a collision course towards the animal remain unclear. Here we show by single unit recording that there exist three classes of looming‐sensitive neurons in the pigeon tectal layer 13, which sends looming information to the nucleus rotundus or to the tectopontine system. The response onset time of tau cells is approximately constant whereas that for rho and eta cells depends on the square root of the diameter/velocity ratio of objects looming towards the animal, the cardioacceleration of which is also linearly related to the square root of this ratio. The receptive field of tectal cells is composed of an excitatory center and an inhibitory periphery, and this periphery does not inhibit responses to looming stimuli. These results suggest that three classes of tectal neurons are specified for detecting an object approaching on a collision course towards the animal, and that rho and eta cells may signal early warning of impending collision whereas tau cells initiate avoidance responses at a constant time before collision through the tectopontine system.

[1]  H. Karten,et al.  A stereotaxic atlas of the brain of the pigeon (Columba livia) , 1967 .

[2]  Hellon Rf The marking of electrode tip positions in nervous tissue. , 1971 .

[3]  R. Hellon The marking of electrode tip positions in nervous tissue. , 1971, The Journal of physiology.

[4]  D. Jassik-Gerschenfeld,et al.  Visual receptive fields of single cells in the pigeon's optic tectum. , 1972, Brain research.

[5]  A. Pearlman,et al.  Single unit receptive fields and the cellular layers of the pigeon optic tectum. , 1974, Brain research.

[6]  H. Karten,et al.  Organization of the tectofugal visual pathway in the pigeon: A retrograde transport study , 1976, The Journal of comparative neurology.

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

[8]  M. Mayer,et al.  Revised nomenclature. , 1980, Journal of immunology.

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

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

[11]  S. J. Phillips,et al.  Head orientation in pigeons: postural, locomotor and visual determinants. , 1989, Brain, behavior and evolution.

[12]  P. Dean,et al.  Event or emergency? Two response systems in the mammalian superior colliculus , 1989, Trends in Neurosciences.

[13]  L. Britto,et al.  Visual telencephalon modulates directional selectivity of accessory optic neurons in pigeons , 1990, Visual Neuroscience.

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

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

[16]  B. Frost,et al.  Visual processing in pigeon nucleus rotundus: Luminance, color, motion, and looming subdivisions , 1993, Visual Neuroscience.

[17]  M. Brandão,et al.  Neural substrate of defensive behavior in the midbrain tectum , 1994, Neuroscience & Biobehavioral Reviews.

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

[19]  H. Bischof,et al.  On the structure and function of the tectofugal visual pathway in laterally eyed birds. , 1997, European journal of morphology.

[20]  Ewert Jp,et al.  Neural correlates of key stimulus and releasing mechanism : a case study and two concepts , 1997 .

[21]  H. Karten,et al.  Two distinct populations of tectal neurons have unique connections within the retinotectorotundal pathway of the pigeon (Columba livia) , 1997, The Journal of comparative neurology.

[22]  H. Karten,et al.  Bottlebrush dendritic endings and large dendritic fields: Motion‐detecting neurons in the tectofugal pathway , 1998, The Journal of comparative neurology.

[23]  P. Perona,et al.  Where is the sun? , 1998, Nature Neuroscience.

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

[25]  L. Rogers,et al.  Organisation of the tectorotundal and SP/IPS‐rotundal projections in the chick , 1998 .

[26]  Hongfeng Gao,et al.  Receptive field properties of visual neurons in the avian nucleus lentiformis mesencephali , 1998, Experimental Brain Research.

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

[28]  A. N. Bowers,et al.  Visual circuits of the avian telencephalon: evolutionary implications , 1999, Behavioural Brain Research.

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

[30]  Yuan Wang,et al.  Regional Variation in Receptive Field Properties of Tectal Neurons in Pigeons , 2000, Brain, Behavior and Evolution.

[31]  Y. Wang,et al.  Excitatory and inhibitory receptive fields of tectal cells are differentially modified by magnocellular and parvocellular divisions of the pigeon nucleus isthmi , 2000, Journal of Comparative Physiology A.

[32]  O. Güntürkün,et al.  Structural organization of parallel information processing within the tectofugal visual system of the pigeon , 2001, The Journal of comparative neurology.

[33]  Shurong Wang,et al.  Receptive field organization and response properties of visual neurons in the pigeon nucleus semilunaris , 2002, Neuroscience Letters.

[34]  H. Karten,et al.  Spatial organization of the pigeon tectorotundal pathway: An interdigitating topographic arrangement , 2003, The Journal of comparative neurology.

[35]  Yong Gu,et al.  Visual Neurons in the Pigeon Brain Encode the Acceleration of Stimulus Motion , 2004, The Journal of Neuroscience.

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

[37]  Gerald E. Hough,et al.  Revised nomenclature for avian telencephalon and some related brainstem nuclei , 2004, The Journal of comparative neurology.

[38]  Hong-Jin Sun,et al.  Chapter 2 The biological bases of time-to-collision computation , 2004 .

[39]  O. Güntürkün,et al.  Tectal mosaic: Organization of the descending tectal projections in comparison to the ascending tectofugal pathway in the pigeon , 2004, The Journal of comparative neurology.

[40]  M. Spetch,et al.  A Dissociation of Motion and Spatial-Pattern Vision in the Avian Telencephalon: Implications for the Evolution of “Visual Streams” , 2004, The Journal of Neuroscience.