Local and Large-Range Inhibition in Feature Detection

Lateral inhibition is perhaps the most ubiquitous of neuronal mechanisms, having been demonstrated in early stages of processing in many different sensory pathways of both mammals and invertebrates. Recent work challenges the long-standing view that assumes that similar mechanisms operate to tune neuronal responses to higher order properties. Scant evidence for lateral inhibition exists beyond the level of the most peripheral stages of visual processing, leading to suggestions that many features of the tuning of higher order visual neurons can be accounted for by the receptive field and other intrinsic coding properties of visual neurons. Using insect target neurons as a model, we present unequivocal evidence that feature tuning is shaped not by intrinsic properties but by potent spatial lateral inhibition operating well beyond the first stages of visual processing. In addition, we present evidence for a second form of higher-order spatial inhibition—a long-range interocular transfer of information that we argue serves a role in establishing interocular rivalry and thus potentially a neural substrate for directing attention to single targets in the presence of distracters. In so doing, we demonstrate not just one, but two levels of spatial inhibition acting beyond the level of peripheral processing.

[1]  David O'Carroll,et al.  Feature-detecting neurons in dragonflies , 1993, Nature.

[2]  Robert M. Olberg,et al.  Identified target-selective visual interneurons descending from the dragonfly brain , 1986, Journal of Comparative Physiology A.

[3]  G. Horridge The Compound eye and vision of insects , 1975 .

[4]  Paul D. Barnett,et al.  Insect Detection of Small Targets Moving in Visual Clutter , 2006, PLoS biology.

[5]  D. C. O'Carroll,et al.  Local feedback mediated via amacrine cells in the insect optic lobe , 2004, Journal of Comparative Physiology A.

[6]  Liza Gross Charting the Spread of Salmonella Infection , 2006, PLoS biology.

[7]  K. N. Leibovic,et al.  Information Processing in the Visual Systems of Arthropods , 1974 .

[8]  R. Olberg,et al.  Eye movements and target fixation during dragonfly prey-interception flights , 2007, Journal of Comparative Physiology A.

[9]  P. C. Murphy,et al.  Corticofugal feedback influences the generation of length tuning in the visual pathway , 1987, Nature.

[10]  G A Horridge,et al.  The separation of visual axes in apposition compound eyes. , 1978, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[11]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[12]  M. Land Visual acuity in insects. , 1997, Annual review of entomology.

[13]  T. Collett,et al.  Vision during flight , 1975 .

[14]  Simon B. Laughlin,et al.  Neural integration in the first optic neuropile of dragonflies , 2004, Journal of comparative physiology.

[15]  D. Ferster,et al.  Membrane Potential and Conductance Changes Underlying Length Tuning of Cells in Cat Primary Visual Cortex , 2001, The Journal of Neuroscience.

[16]  Bart R. H. Geurten,et al.  Neural mechanisms underlying target detection in a dragonfly centrifugal neuron , 2007, Journal of Experimental Biology.

[17]  Karin Nordström,et al.  Feature detection and the hypercomplex property in insects , 2009, Trends in Neurosciences.

[18]  N. Strausfeld Atlas of an Insect Brain , 1976, Springer Berlin Heidelberg.

[19]  M. May,et al.  Foraging behavior ofPachydiplax longipennis (Odonata: Libellulidae) , 1997, Journal of Insect Behavior.

[20]  C. H. Fraser Rowell,et al.  The neuronal basis of a sensory analyser, the acridid movement detector system. IV. The preference for small field stimuli. , 1977, The Journal of experimental biology.

[21]  Karin Nordström,et al.  Small object detection neurons in female hoverflies , 2006, Proceedings of the Royal Society B: Biological Sciences.

[22]  Simon B. Laughlin,et al.  Neural integration in the first optic neuropile of dragonflies , 1976, Journal of comparative physiology.

[23]  Robert M. Olberg,et al.  Object- and self-movement detectors in the ventral nerve cord of the dragonfly , 1981, Journal of comparative physiology.

[24]  David C. O'Carroll,et al.  Retinotopic Organization of Small-Field-Target-Detecting Neurons in the Insect Visual System , 2007, Current Biology.

[25]  Andrew D. Straw,et al.  Vision Egg: an Open-Source Library for Realtime Visual Stimulus Generation , 2008, Frontiers Neuroinformatics.

[26]  R. Olberg,et al.  Prey size selection and distance estimation in foraging adult dragonflies , 2005, Journal of Comparative Physiology A.

[27]  THOMAS COLLETT,et al.  Visual Neurones for Tracking Moving Targets , 1971, Nature.

[28]  M. May,et al.  Fights at the Dinner Table: Agonistic Behavior in Pachydiplax longipennis (Odonata: Libellulidae) at Feeding Sites , 2003, Journal of Insect Behavior.

[29]  Patrick A. Shoemaker,et al.  A Model for the Detection of Moving Targets in Visual Clutter Inspired by Insect Physiology , 2008, PloS one.

[30]  Nicholas J. Priebe,et al.  Inhibition, Spike Threshold, and Stimulus Selectivity in Primary Visual Cortex , 2008, Neuron.

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

[32]  S. Laughlin,et al.  Predictive coding: a fresh view of inhibition in the retina , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.