Neural processing of imminent collision in humans

Detecting a looming object and its imminent collision is imperative to survival. For most humans, it is a fundamental aspect of daily activities such as driving, road crossing and participating in sport, yet little is known about how the brain both detects and responds to such stimuli. Here we use functional magnetic resonance imaging to assess neural response to looming stimuli in comparison with receding stimuli and motion-controlled static stimuli. We demonstrate for the first time that, in the human, the superior colliculus and the pulvinar nucleus of the thalamus respond to looming in addition to cortical regions associated with motor preparation. We also implicate the anterior insula in making timing computations for collision events.

[1]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

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

[3]  Jon H. Kaas,et al.  Pulvinar contributions to the dorsal and ventral streams of visual processing in primates , 2007, Brain Research Reviews.

[4]  Kenneth F. Valyear,et al.  Human parietal cortex in action , 2006, Current Opinion in Neurobiology.

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

[6]  John P. Wann,et al.  Perceiving Time to Collision Activates the Sensorimotor Cortex , 2005, Current Biology.

[7]  Peter Redgrave,et al.  A direct projection from superior colliculus to substantia nigra for detecting salient visual events , 2003, Nature Neuroscience.

[8]  Norbert Kathmann,et al.  Neural correlates of error awareness , 2007, NeuroImage.

[9]  K. Grieve,et al.  The primate pulvinar nuclei: vision and action , 2000, Trends in Neurosciences.

[10]  Shurong Wang,et al.  Tectal neurons signal impending collision of looming objects in the pigeon , 2005, The European journal of neuroscience.

[11]  Cathy Craig,et al.  Using Time-to-Contact Information to Assess Potential Collision Modulates Both Visual and Temporal Prediction Networks , 2008, Frontiers in human neuroscience.

[12]  Sabine Kastner,et al.  Visual attention as a multilevel selection process , 2004, Cognitive, affective & behavioral neuroscience.

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

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

[15]  J. Gibson.  Visually controlled locomotion and visual orientation in animals. , 1998, British journal of psychology.

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

[17]  Anthony M. Norcia,et al.  Development of sensitivity to information for impending collision , 1977 .

[18]  P. Redgrave,et al.  The basal ganglia: a vertebrate solution to the selection problem? , 1999, Neuroscience.

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

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

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

[22]  R. Walker,et al.  Functional Imaging of the Human Superior Colliculus: An Optimised Approach , 2009, NeuroImage.

[23]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[24]  Mark S. Cohen,et al.  Spatiotopic Organization in Human Superior Colliculus Observed with fMRI , 2000, NeuroImage.

[25]  B. Stein,et al.  Multimodal Representation in the Superior Colliculus and Optic Tectum , 1984 .

[26]  Matthew B. Wall,et al.  Time perception: Manipulation of task difficulty dissociates clock functions from other cognitive demands , 2007, Neuropsychologia.

[27]  A. Opstal,et al.  Stimulus intensity modifies saccadic reaction time and visual response latency in the superior colliculus , 2006, Experimental Brain Research.

[28]  David M Jacobs,et al.  Judgements of time to contact are affected by rate of appearance of visible texture , 2010, Quarterly journal of experimental psychology.