logo biblio digital exactas
logo twitter logo instagram logo whatsapp logo mail

Navegar

Colección

Datos Estadísticas

Artículo

Este artículo es de Acceso Abierto y puede ser descargado en su versión final desde nuestro repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Arthropods are diverse, abundant, successful animals that exploit all available ecological niches. They sense the environment,move, interact with prey/predators/conspecifics, learn, and so forth using small brains with five orders of magnitude less neuronsthan mammals. Hence, these brains need to be efficient in information processing. One distinct aspect is the presence of large,easily identifiable single neurons that act as functional units for information processing integrating a high volume of informationfrom different sources to guide behavior. To understand the synaptic organization behind these high-integration nodes researchon suitable neurons is needed. The lobula giant neurons (LGs) found in the third optic neuropil, the lobula, of semiterrestrial crabsNeohelice granulata respond to moving stimuli, integrate information from both eyes, and show short- and long-term plasticity.They are thought to be key elements in the visuomotor transformation guiding escape responses to approaching objects. Onesubgroup, the MLG1 (monostratified LG type 1), is composed of 16 elements that have very wide main branches and a regulararrangement in a deep layer of the lobula which allows their identification even in unstained preparations. Here, we describethe types and abundance of synaptic contacts involving MLG1 profiles using transmission electron microscopy (TEM). We foundan unexpected diversity of synaptic motifs and an apparent compartmentalization of the dendritic arbor in two domains whereMLG1s act predominantly as presynaptic or postsynaptic, respectively. We propose that the variety of contact types found in thedendritic arbor of the MLG1s reflects the multiple circuits in which these cells are involved. Regarding the detection of approachingobjects, the distinctive input contact motifs shared by lobula giant neurons in crabs and locusts suggest a similar organization ofthe collision-detecting pathways in both species.

Registro:

Documento: Artículo
Título:The Synaptic Complexity of a High-Integration Lobula Giant Neuron in Crabs
Autor:Barnatan, Yair; Rind, Claire; Scarano, Florencia; Sztarker, Julieta
Filiación:Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Idioma:eng
Palabras clave:arthropod; chemical synapses; collision detection; giant neurons; lobula circuits; visual systems
Año:2024
Volumen:533
Número:2
Página de inicio:e70026
DOI: http://dx.doi.org/10.1002/cne.70026
Título revista:Journal of Comparative Neurology
Título revista abreviado:J Comp Neurol
ISSN:0021-9967
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00219967_v533_n2_pe70026_Barnatan.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00219967_v533_n2_pe70026_Barnatan

Referencias:

  • Ache, J. M., J. Polsky, S. Alghailani, et al. 2019. “Neural Basis for Looming Size and Velocity Encoding in the Drosophila Giant Fiber Escape Pathway.” Current Biology 29: 1073–1081.e4
  • Ammer, G., E. Serbe‐Kamp, A. S. Mauss, F. G. Richter, S. Fendl, and A. Borst. 2023. “Multilevel Visual Motion Opponency in Drosophila.” Nature Neuroscience 26: 1894–1905
  • Berón de Astrada, M., and D. Tomsic. 2002. “Physiology and Morphology of Visual Movement Detector Neurons in a Crab (Decapoda: Brachyura).” Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 188: 539–551
  • Borst, A., and L. N. Groschner. 2023. “How Flies See Motion.” Annual Review of Neuroscience 46: 17–37
  • Buhmann, J., A. Sheridan, C. Malin‐Mayor, et al. 2021. “Automatic Detection of Synaptic Partners in a Whole‐Brain Drosophila Electron Microscopy Data Set.” Nature Methods 18: 771–774
  • Cocks, E. T. 2021. “Use of Serial Block Face‐Scanning Electron Microscopy to Study the Ultrastructure of Vertebrate and Invertebrate Biology.” PhD Thesis, Newcastle University
  • Dombrovski, M., M. Y. Peek, J.‐Y. Park, et al. 2023. “Synaptic Gradients Transform Object Location to Action.” Nature 613: 534–542
  • Dorkenwald, S., A. Matsliah, A. R. Sterling, et al. 2024. “Neuronal Wiring Diagram of an Adult Brain.” Nature 634: 124–138
  • Eckstein, N., A. S. Bates, A. Champion, et al. 2024. “Neurotransmitter Classification From Electron Microscopy Images at Synaptic Sites in Drosophila Melanogaster.” Cell 187: 2574–2594.e23
  • Fathala, M. D. V., and H. Maldonado. 2011. “Shelter Use During Exploratory and Escape Behaviour of the Crab Chasmagnathus Granulatus: A Field Study.” Journal of Ethology 29: 263–273
  • Fotowat, H., R. R. Harrison, and F. Gabbiani. 2011. “Multiplexing of Motor Information in the Discharge of a Collision Detecting Neuron During Escape Behaviors.” Neuron 69: 147–158
  • Hafner, G. S. 1973. “The Neural Organization of the Lamina Ganglionaris in the Crayfish: A Golgi and EM Study.” Journal of Comparative Neurology 152: 255–280
  • Hafner, G. S. 1974. “The Ultrastructure of Retinula Cell Endings in the Compound Eye of the Crayfish.” Journal of Neurocytology 3: 295–311
  • Hatsopoulos, N., F. Gabbiani, and G. Laurent. 1995. “Elementary Computation of Object Approach by Wide‐Field Visual Neuron.” Science 270: 1000–1003
  • Kilman, V. L., and E. Marder. 1996. “Ultrastructure of the Stomatogastric Ganglion Neuropil of the Crab, Cancer borealis.” Journal of Comparative Neurology 374: 362–375
  • Kim, H., H. Park, J. Lee, and A. J. Kim. 2023. “A Visuomotor Circuit for Evasive Flight Turns in Drosophila.” Current Biology: CB 33: 321–335.e6
  • King, D. G. 1976. “Organization of Crustacean Neuropil. I. Patterns of Synaptic Connections in Lobster Stomatogastric Ganglion.” Journal of Neurocytology 5: 207–237
  • Klapoetke, N. C., A. Nern, M. Y. Peek, et al. 2017. “Ultra‐Selective Looming Detection From Radial Motion Opponency.” Nature 551: 237–241
  • Klapoetke, N. C., A. Nern, E. M. Rogers, G. M. Rubin, M. B. Reiser, and G. M. Card. 2022. “A Functionally Ordered Visual Feature Map in the Drosophila Brain.” Neuron 110: 1700–1711.e6
  • Lepore, M. G., D. Tomsic, and J. Sztarker. 2022. “Neural Organization of the Third Optic Neuropil, the Lobula, in the Highly Visual Semiterrestrial Crab Neohelice granulata.” Journal of Comparative Neurology 530, no. 10: 1533–1550
  • Liu, W. W., and R. I. Wilson. 2013. “Glutamate is an Inhibitory Neurotransmitter in the Drosophila Olfactory System.” Proc Natl Acad Sci USA 110: 10294–10299
  • Matsliah, A., S. Yu, K. Kruk, et al. 2024. “Neuronal Parts List and Wiring Diagram for a Visual System.” Nature 634: 166–180
  • Medan, V., M. Berón De Astrada, F. Scarano, and D. Tomsic. 2015. “A Network of Visual Motion‐Sensitive Neurons for Computing Object Position in an Arthropod.” Journal of Neuroscience: The Official Journal of the Society for Neuroscience 35: 6654–6666
  • Medan, V., D. Oliva, and D. Tomsic. 2007. “Characterization of Lobula Giant Neurons Responsive to Visual Stimuli That Elicit Escape Behaviors in the Crab Chasmagnathus.” Journal of Neurophysiology 98: 2414–2428
  • Mizunami, M., F. Yokohari, and M. Takahata. 2004. “Further Exploration Into the Adaptive Design of the Arthropod “Microbrain”: I. Sensory and Memory‐Processing Systems.” Zoological Science 21: 1141–1151
  • Morimoto, M. M., A. Nern, A. Zhao, et al. 2020. “Spatial Readout of Visual Looming in the Central Brain of Drosophila.” Elife 9: e57685
  • Nässel, D. R., and T. H. Waterman. 1977. “Golgi EM Evidence for Visual Information Channelling in the Crayfish Lamina Ganglionaris.” Brain Research 130: 556–563
  • Nässel, D. R. 1975. “The Organization of the Lamina Ganglionaris of the Prawn, Pandalus Borealis (Kröyer).” Cell and Tissue Research 163: 445–464
  • Nässel, D. R. 1977. “Types and Arrangements of Neurons in the Crayfish Optic Lamina.” Cell and Tissue Research 179: 45–75
  • Nässel, D. R., R. Elofsson, and R. Odselius. 1978. “Neuronal Connectivity Patterns in the Compound Eyes of Artemia salina and Daphnia magna (Crustacea: Branchiopoda).” Cell and Tissue Research 190: 435–437
  • Oliva, D., V. Medan, and D. Tomsic. 2007. “Escape Behavior and Neuronal Responses to Looming Stimuli in the Crab Chasmagnathus Granulatus (Decapoda: Grapsidae).” Journal of Experimental Biology 210: 865–880
  • Oliva, D., and D. Tomsic. 2012. “Visuo‐Motor Transformations Involved in the Escape Response to Looming Stimuli in the Crab Neohelice ( = Chasmagnathus) granulata.” Journal of Experimental Biology 215: 3488–3500
  • Oliva, D., and D. Tomsic. 2014. “Computation of Object Approach by a System of Visual Motion‐Sensitive Neurons in the Crab Neohelice.” Journal of Neurophysiology 112: 1477–1490
  • Oliva, D., and D. Tomsic. 2016. “Object Approach Computation by a Giant Neuron and Its Relationship With the Speed of Escape in the Crab Neohelice.” Journal of Experimental Biology 219: 3339–3352
  • Preuss, T., P. E. Osei‐Bonsu, S. A. Weiss, C. Wang, and D. S. Faber. 2006. “Neural Representation of Object Approach in a Decision‐Making Motor Circuit.” Journal of Neuroscience: The Official Journal of the Society for Neuroscience 26: 3454–3464
  • Qin, B., T. H. Humberg, A. Kim, et al. 2019. “Muscarinic Acetylcholine Receptor Signaling Generates OFF Selectivity in a Simple Visual Circuit.” Nat Commun 10: 4093
  • R Core Team. 2022. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R‐project.org/
  • von Reyn, C. R. 2022. “Feature Encoding: How Back‐to‐Front Motion Guides the Polite Fly.” Current Biology 32: R513–R515
  • von Reyn, C. R., A. Nern, W. R. Williamson, et al. 2017. “Feature Integration Drives Probabilistic Behavior in the Drosophila Escape Response.” Neuron 94: 1190–1204.e6
  • Rind, F. C. 1996. “Intracellular Characterization of Neurons in the Locust Brain Signaling Impending Collision.” Journal of Neurophysiology 75: 986–995
  • Rind, F. C., and D. I. Bramwell. 1996. “Neural Network Based on the Input Organization of an Identified Neuron Signaling Impending Collision.” Journal of Neurophysiology 75: 967–985
  • Rind, F. C., and G. Leitinger. 2000. “Immunocytochemical Evidence That Collision Sensing Neurons in the Locust Visual System Contain Acetylcholine.” Journal of Comparative Neurology 423: 389–401
  • Rind, F. C., and P. J. Simmons. 1992. “Orthopteran DCMD Neuron: A Reevaluation of Responses to Moving Objects. I. Selective Responses to Approaching Objects.” Journal of Neurophysiology 68: 1654–1666
  • Rind, F. C., and P. J. Simmons. 1997. “Signaling of Object Approach by the DCMD Neuron of the Locust.” Journal of Neurophysiology 77: 1029–1033
  • Rind, F. C., and P. J. Simmons. 1998. “Local Circuit for the Computation of Object Approach by an Identified Visual Neuron in the Locust.” Journal of Comparative Neurology 395: 405–415
  • Rind, F. C., S. Wernitznig, P. Pölt, et al. 2016. “Two Identified Looming Detectors in the Locust: Ubiquitous Lateral Connections Among Their Inputs Contribute to Selective Responses to Looming Objects.” Scientific Reports 6: 35525
  • Rosner, R., J. von Hadeln, T. Salden, and U. Homberg. 2017. “Anatomy of the Lobula Complex in the Brain of the Praying Mantis Compared to the Lobula Complexes of the Locust and Cockroach.” Journal of Comparative Neurology 525: 2343–2357
  • Sal Moyano, M. P., M. A. Gavio, and T. A Luppi. 2012. “Mating System of the Burrowing Crab Neohelice granulata (Brachyura: Varunidae) in Two Contrasting Environments: Effect of Burrow Architecture.” Marine Biology 159: 1403–1416
  • Sal Moyano, M. P., M. Lorusso, J. Nuñez, P. Ribeiro, M. A. Gavio, and T. Luppi. 2016. “Male Size‐Dependent Dominance for Burrow Holding in the Semiterrestrial Crab Neohelice granulata: Multiple Tactics Used by Intermediate‐Sized Males.” Behavioral Ecology and Sociobiology 70: 1497–1505
  • Santer, R. D., F. C. Rind, R. Stafford, and P. J. Simmons. 2006. “Role of an Identified Looming‐Sensitive Neuron in Triggering a Flying Locust's Escape.” Journal of Neurophysiology 95: 3391–3400
  • Sattelle, D. B. 1980. “Acetylcholine Receptors of Insects.” In Advances in Insect Physiology, edited by M. J. Berridge, J. E. Treherne, and V. B. Wigglesworth, 215–315. Academic Press. https://www.sciencedirect.com/science/article/pii/S0065280608601423
  • Scarano, F., J. Sztarker, V. Medan, M. Berón de Astrada, and D. Tomsic. 2018. “Binocular Neuronal Processing of Object Motion in an Arthropod.” Journal of Neuroscience: The Official Journal of the Society for Neuroscience 38, no. 31: 6933–6948
  • Scheffer, L. K., C. S. Xu, M. Januszewski, et al. 2020. “A Connectome and Analysis of the Adult Drosophila Central Brain.” Elife 9: e57443
  • Schürmann, F.‐W. 2016. “Fine Structure of Synaptic Sites and Circuits in Mushroom Bodies of Insect Brains.” Arthropod Structure 45: 399–421
  • Simmons, P. J., and F. C. Rind. 1992. “Orthopteran DCMD Neuron: A Reevaluation of Responses to Moving Objects. II. Critical Cues for Detecting Approaching Objects.” Journal of Neurophysiology 68: 1667–1682
  • Sun, H., and B. J. Frost. 1998. “Computation of Different Optical Variables of Looming Objects in Pigeon Nucleus Rotundus Neurons.” Nature Neuroscience 1: 296–303
  • Sztarker, J., N. J. Strausfeld, and D. Tomsic. 2005. “Organization of Optic Lobes That Support Motion Detection in a Semiterrestrial Crab.” Journal of Comparative Neurology 493: 396–411
  • Sztarker, J., and D. Tomsic. 2004. “Binocular Visual Integration in the Crustacean Nervous System.” Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 190: 951–962
  • Sztarker, J., and D. Tomsic. 2008. “Neuronal Correlates of the Visually Elicited Escape Response of the Crab Chasmagnathus Upon Seasonal Variations, Stimuli Changes and Perceptual Alterations.” Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 194: 587–596
  • Sztarker, J., and D. Tomsic. 2011. “Brain Modularity in Arthropods: Individual Neurons That Support “What” But Not “Where” Memories.” Journal of Neuroscience: The Official Journal of the Society for Neuroscience 31: 8175–8180
  • Tanaka, R., and D. A. Clark. 2022. “Neural Mechanisms to Exploit Positional Geometry for Collision Avoidance.” Current Biology: CB 32: 2357–2374.e6
  • Tomsic, D. 2016. “Visual Motion Processing Subserving Behavior in Crabs.” Current Opinion in Neurobiology 41: 113–121
  • Tomsic, D., M. Berón de Astrada, and J. Sztarker. 2003. “Identification of Individual Neurons Reflecting Short‐ and Long‐Term Visual Memory in an Arthropodo.” Journal of Neuroscience: The Official Journal of the Society for Neuroscience 23: 8539–8546
  • Tomsic, D., J. Sztarker, M. Berón de Astrada, D. Oliva, and E. Lanza. 2017. “The Predator and Prey Behaviors of Crabs: From Ecology to Neural Adaptations.” Journal of Experimental Biology 220: 2318–2327
  • Trimmer, B. A. 1995. “Current Excitement From Insect Muscarinic Receptors.” Trends in Neuroscience (Tins) 18: 104–111
  • Uchizono, K. 1967. “Inhibitory Synapses on the Stretch Receptor Neurone of the Crayfish.” Nature 214: 833–834
  • de Vries, S. E. J., and T. R. Clandinin. 2012. “Loom‐Sensitive Neurons Link Computation to Action in the Drosophila Visual System.” Current Biology: CB 22: 353–362
  • Watson, A. H. 1988. “Antibodies Against GABA and Glutamate Label Neurons With Morphologically Distinct Synaptic Vesicles in the Locust Central Nervous System.” Neuroscience 26: 33–44
  • Watson, A. H. D., and F.‐W. Schürmann. 2002. “Synaptic Structure, Distribution, and Circuitry in the Central Nervous System of the Locust and Related Insects.” Microscopy Research and Technique 56: 210–226
  • Wernitznig, S., F. C. Rind, A. Zankel, et al. 2022. “The Complex Synaptic Pathways Onto a Looming‐Detector Neuron Revealed Using Serial Block‐Face Scanning Electron Microscopy.” Journal of Comparative Neurology 530: 518–536
  • Wilson, E. O. 1988. Biodiversity (521 p). Washington: National Academy Press
  • Wu, M., A. Nern, W. R. Williamson, et al. 2016. “Visual Projection Neurons in the Drosophila Lobula Link Feature Detection to Distinct Behavioral Programs.” Elife 5: e21022
  • Zhu, Y., R. B. Dewell, H. Wang, and F. Gabbiani. 2018. “Pre‐Synaptic Muscarinic Excitation Enhances the Discrimination of Looming Stimuli in a Collision‐Detection Neuron.” Cell Reports 23: 2365–2378.

Citas:

---------- APA ----------
Barnatan, Yair, Rind, Claire, Scarano, Florencia & Sztarker, Julieta (2024) . The Synaptic Complexity of a High-Integration Lobula Giant Neuron in Crabs. Journal of Comparative Neurology, 533(2), e70026.
http://dx.doi.org/10.1002/cne.70026
---------- CHICAGO ----------
Barnatan, Yair, Rind, Claire, Scarano, Florencia, Sztarker, Julieta. "The Synaptic Complexity of a High-Integration Lobula Giant Neuron in Crabs" . Journal of Comparative Neurology 533, no. 2 (2024) : e70026.
http://dx.doi.org/10.1002/cne.70026
---------- MLA ----------
Barnatan, Yair, Rind, Claire, Scarano, Florencia, Sztarker, Julieta. "The Synaptic Complexity of a High-Integration Lobula Giant Neuron in Crabs" . Journal of Comparative Neurology, vol. 533, no. 2, 2024, pp. e70026.
http://dx.doi.org/10.1002/cne.70026
---------- VANCOUVER ----------
Barnatan, Yair, Rind, Claire, Scarano, Florencia, Sztarker, Julieta. The Synaptic Complexity of a High-Integration Lobula Giant Neuron in Crabs. J Comp Neurol. 2024;533(2):e70026.
http://dx.doi.org/10.1002/cne.70026