A Network of Visual Motion-Sensitive Neurons for Computing Object Position in an Arthropod

Highly active insects and crabs depend on visual motion information for detecting and tracking mates, prey, or predators, for which they require directional control systems containing internal maps of visual space. A neural map formed by large, motion-sensitive neurons implicated in processing panoramic flow is known to exist in an optic ganglion of the fly. However, an equivalent map for processing spatial positions of single objects has not been hitherto identified in any arthropod. Crabs can escape directly away from a visual threat wherever the stimulus is located in the 360° field of view. When tested in a walking simulator, the crab Neohelice granulata immediately adjusts its running direction after changes in the position of the visual danger stimulus smaller than 1°. Combining mass and single-cell staining with in vivo intracellular recording, we show that a particular class of motion-sensitive neurons of the crab's lobula that project to the midbrain, the monostratified lobula giants type 1 (MLG1), form a system of 16 retinotopically organized elements that map the 360° azimuthal space. The preference of these neurons for horizontally moving objects conforms the visual ecology of the crab's mudflat world. With a mean receptive field of 118°, MLG1s have a large superposition among neighboring elements. Our results suggest that the MLG1 system conveys information on object position as a population vector. Such computational code can enable the accurate directional control observed in the visually guided behaviors of crabs.

• Publication year

  2015

• Venue

  Journal of Neuroscience

• Publication date

  2015-04-29

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1523/JNEUROSCI.4667-14.2015PMID 25926445PMCID PMC6605188
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Escape response of the crab Neohelice to computer generated looming and translational visual danger stimuli.

  2014influential reference
• Near-Optimal Decoding of Transient Stimuli from Coupled Neuronal Subpopulations

  2014cited by this paper
• Fly visual course control: behaviour, algorithms and circuits

  2014cited by this paper
• Motion-detecting circuits in flies: coming into view.

  2014cited by this paper
• Computation of object approach by a system of visual motion-sensitive neurons in the crab Neohelice.

  2014influential reference
• From the Cover: Eight pairs of descending visual neurons in the dragonfly give wing motor centers accurate population vector of prey direction

  2013cited by this paper
• Texture dependence of motion sensing and free flight behavior in blowflies

  2013cited by this paper
• Plasticity in the Arthropod Optic Lobes Martı́n

  2013cited by this paper
• Widespread Sensitivity to Looming Stimuli and Small Moving Objects in the Central Complex of an Insect Brain

  2013cited by this paper
• Visuo-motor transformations involved in the escape response to looming stimuli in the crab Neohelice (=Chasmagnathus) granulata

  2012influential reference
• The neuroethology of escape in crabs: from sensory ecology to neurons and back.

  2012cited by this paper
• Escape behavior: linking neural computation to action.

  2012cited by this paper
• Regionalization in the eye of the grapsid crab Neohelice granulata (=Chasmagnathus granulatus): variation of resolution and facet diameters

  2011influential reference
• How visual space maps in the optic neuropils of a crab

  2011cited by this paper
• Brain Modularity in Arthropods: Individual Neurons That Support “What” But Not “Where” Memories

  2011cited by this paper
• Neural Action Fields for Optic Flow Based Navigation: A Simulation Study of the Fly Lobula Plate Network

  2011cited by this paper
• Brain organization and the origin of insects: an assessment

  2009cited by this paper
• Neuronal correlates of the visually elicited escape response of the crab Chasmagnathus upon seasonal variations, stimuli changes and perceptual alterations

  2008cited by this paper
• Characterisation of a blowfly male-specific neuron using behaviourally generated visual stimuli

  2007cited by this paper
• Escape behavior and neuronal responses to looming stimuli in the crab Chasmagnathus granulatus (Decapoda: Grapsidae)

  2007influential reference
• Maplike Representation of Celestial E-Vector Orientations in the Brain of an Insect

  2007cited by this paper
• Relationship between the Phases of Sensory and Motor Activity during a Looming-Evoked Multistage Escape Behavior

  2007cited by this paper
• Faculty Opinions recommendation of Maplike representation of celestial E-vector orientations in the brain of an insect.

  2007cited by this paper
• Characterization of lobula giant neurons responsive to visual stimuli that elicit escape behaviors in the crab Chasmagnathus.

  2007influential reference
• Insect Detection of Small Targets Moving in Visual Clutter

  2006cited by this paper
• Organization of optic lobes that support motion detection in a semiterrestrial crab

  2005influential reference
• Population coding of self-motion: applying bayesian analysis to a population of visual interneurons in the fly.

  2005cited by this paper
• Binocular visual integration in the crustacean nervous system

  2004cited by this paper
• Identification of Individual Neurons Reflecting Short- and Long-Term Visual Memory in an Arthropodo

  2003influential reference
• Physiology and morphology of visual movement detector neurons in a crab (Decapoda: Brachyura)

  2002cited by this paper
• Population Vector Coding by the Giant Interneurons of the Cockroach

  2000influential reference
• Single Units and Visual Cortical Organization

  1998cited by this paper
• A neuronal network for computing population vectors in the leech

  1998cited by this paper
• A glimpse into crabworld.

  1997cited by this paper
• The variation of resolution and of ommatidial dimensions in the compound eyes of the fiddler crab Uca lactea annulipes (Ocypodidae, Brachyura, Decapoda)

  1996cited by this paper
• The visual control of behaviour in fiddler crabs

  1995influential reference
• Neural mechanisms for forming a perceptual decision.

  1994influential reference
• Eye movements in freely moving crabs: Their sensory basis and possible role in flow-field analysis

  1993cited by this paper
• Descending pathways connecting the male-specific visual system of flies to the neck and flight motor

  1991cited by this paper
• Structural organization of male-specific visual neurons in calliphorid optic lobes

  1991cited by this paper
• Visually Elicited Escape in Crabs

  1990cited by this paper
• Spatial Vision in a Flat World: Optical and Neural Adaptations in Arthropods

  1989cited by this paper
• Neuronal population coding of movement direction.

  1986cited by this paper
• Connexions between a movement-detecting visual interneurone and flight motoneurones of a locust.

  1980cited by this paper
• Discharge patterns and functional organization of mammalian retina.

  1953cited by this paper

• The Synaptic Complexity of a High‐Integration Lobula Giant Neuron in Crabs

  2025influential citation
• Responses of a locust visual interneuron correlate with simple and compound object motion within the vertical plane

  2025cites this paper
• Complex motion trajectories are represented by a population code from the ensemble activity of multiple motion-sensitive descending interneurons in locusts

  2024cites this paper
• Freezing of movements and its correspondence with MLG1 neurons response to looming stimuli in the crab Neohelice.

  2024cites this paper
• Neuroethology in South America: past, present and future.

  2023cites this paper
• Predatory behavior under monocular and binocular conditions in the semiterrestrial crab Neohelice granulata

  2023cites this paper
• A BLG1 neural model implements the unique looming selectivity to diving target

  2023cites this paper
• Dual Receptive Fields Underlying Target and Wide-Field Motion Sensitivity in Looming-Sensitive Descending Neurons

  2023cites this paper
• A neural strategy for directional behaviour

  2023cites this paper
• Threatening stimuli elicit a sequential cardiac pattern in arthropods

  2023cites this paper
• A Looming Spatial Localization Neural Network Inspired by MLG1 Neurons in the Crab Neohelice

  2022cites this paper
• Accelerating Motion Perception Model Mimics the Visual Neuronal Ensemble of Crab

  2022influential citation
• Matched function of the neuropil processing optic flow in flies and crabs: the lobula plate mediates optomotor responses in Neohelice granulata

  2022cites this paper
• Behavioural and neural responses of crabs show evidence for selective attention in predator avoidance

  2022cites this paper
• Immunocytochemical Localization of Enzymes Involved in Dopamine, Serotonin, and Acetylcholine Synthesis in the Optic Neuropils and Neuroendocrine System of Eyestalks of Paralithodes camtschaticus

  2022cites this paper
• Neural organization of the third optic neuropil, the lobula, in the highly visual semiterrestrial crab Neohelice granulata

  2022influential citation
• Strange eyes, stranger brains: exceptional diversity of optic lobe organization in midwater crustaceans

  2021cites this paper
• Convergent evolution of optic lobe neuropil in Pancrustacea.

  2021cites this paper
• The lobula plate is exclusive to insects.

  2021cites this paper
• Visual determinants of prey chasing behavior in a mudflat crab

  2020cites this paper
• Direction Selective Neurons Responsive to Horizontal Motion in a Crab Reflect an Adaptation to Prevailing Movements in Flat Environments

  2020cites this paper
• Multielectrode Recordings From Identified Neurons Involved in Visually Elicited Escape Behavior

  2020cites this paper
• Unidirectional Optomotor Responses and Eye Dominance in Two Species of Crabs

  2019cites this paper
• Masters of communication: The brain of the banded cleaner shrimp Stenopus hispidus (Olivier, 1811) with an emphasis on sensory processing areas

  2019cites this paper
• A multimodal pathway including the basal ganglia in the feline brain.

  2019cites this paper
• Binocular Neuronal Processing of Object Motion in an Arthropod

  2018cites this paper
• The predator and prey behaviors of crabs: from ecology to neural adaptations

  2017cites this paper
• Object approach computation by a giant neuron and its relationship with the speed of escape in the crab Neohelice

  2016cites this paper
• Data-driven adaptation of the evasion behaviour in fiddler crabs

  2016cites this paper
• Arthropod eyes: The early Cambrian fossil record and divergent evolution of visual systems.

  2016cites this paper
• Predation risk modifies behaviour by shaping the response of identified brain neurons

  2016cites this paper
• Visual motion processing subserving behavior in crabs.

  2016cites this paper
• Comparative analyses of olfactory systems in terrestrial crabs (Brachyura): evidence for aerial olfaction?

  2015cites this paper
• Differences in the escape response of a grapsid crab in the field and in the laboratory

  2015cites this paper