Literature DB >> 31296565

The role of the optic tectum for visually evoked orienting and evasive movements.

Daichi G Suzuki1,2, Juan Pérez-Fernández1, Tobias Wibble1,3, Andreas A Kardamakis1, Sten Grillner4.   

Abstract

As animals forage for food and water or evade predators, they must rapidly decide what visual features in the environment deserve attention. In vertebrates, this visuomotor computation is implemented within the neural circuits of the optic tectum (superior colliculus in mammals). However, the mechanisms by which tectum decides whether to approach or evade remain unclear, and also which neural mechanisms underlie this behavioral choice. To address this problem, we used an eye-brain-spinal cord preparation to evaluate how the lamprey responds to visual inputs with distinct stimulus-dependent motor patterns. Using ventral root activity as a behavioral readout, we classified 2 main types of fictive motor responses: (i) a unilateral burst response corresponding to orientation of the head toward slowly expanding or moving stimuli, particularly within the anterior visual field, and (ii) a unilateral or bilateral burst response triggering fictive avoidance in response to rapidly expanding looming stimuli or moving bars. A selective pharmacological blockade revealed that the brainstem-projecting neurons in the deep layer of the tectum in interaction with local inhibitory interneurons are responsible for selecting between these 2 visually triggered motor actions conveyed through downstream reticulospinal circuits. We suggest that these visual decision-making circuits had evolved in the common ancestor of vertebrates and have been conserved throughout vertebrate phylogeny.

Entities:  

Keywords:  evolution; superior colliculus; visuomotor transformation

Year:  2019        PMID: 31296565      PMCID: PMC6660747          DOI: 10.1073/pnas.1907962116

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  45 in total

1.  Activity of reticulospinal neurons during locomotion in the freely behaving lamprey.

Authors:  T G Deliagina; P V Zelenin; P Fagerstedt; S Grillner; G N Orlovsky
Journal:  J Neurophysiol       Date:  2000-02       Impact factor: 2.714

Review 2.  New perspectives on the evolution of protochordate sensory and locomotory systems, and the origin of brains and heads.

Authors:  T C Lacalli
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2001-10-29       Impact factor: 6.237

3.  Coding of cognitive magnitude: compressed scaling of numerical information in the primate prefrontal cortex.

Authors:  Andreas Nieder; Earl K Miller
Journal:  Neuron       Date:  2003-01-09       Impact factor: 17.173

4.  The neural basis of the Weber-Fechner law: a logarithmic mental number line.

Authors:  Stanislas Dehaene
Journal:  Trends Cogn Sci       Date:  2003-04       Impact factor: 20.229

Review 5.  Biological pattern generation: the cellular and computational logic of networks in motion.

Authors:  Sten Grillner
Journal:  Neuron       Date:  2006-12-07       Impact factor: 17.173

6.  Tectal control of locomotion, steering, and eye movements in lamprey.

Authors:  Kazuya Saitoh; Ariane Ménard; Sten Grillner
Journal:  J Neurophysiol       Date:  2007-02-15       Impact factor: 2.714

7.  Early evolution of multifocal optics for well-focused colour vision in vertebrates.

Authors:  O S E Gustafsson; S P Collin; R H H Kröger
Journal:  J Exp Biol       Date:  2008-05       Impact factor: 3.312

Review 8.  Modeling a vertebrate motor system: pattern generation, steering and control of body orientation.

Authors:  Sten Grillner; Alexander Kozlov; Paolo Dario; Cesare Stefanini; Arianna Menciassi; Anders Lansner; Jeanette Hellgren Kotaleski
Journal:  Prog Brain Res       Date:  2007       Impact factor: 2.453

9.  Dual innervation of the lamprey retina by GABAergic and glutamatergic retinopetal fibers. A quantitative EM immunogold study.

Authors:  J P Rio; J Repérant; N P Vesselkin; N B Kenigfest-Rio; D Miceli
Journal:  Brain Res       Date:  2003-01-10       Impact factor: 3.252

Review 10.  Evolution of brains, cognition, and consciousness.

Authors:  Ann B Butler
Journal:  Brain Res Bull       Date:  2007-11-20       Impact factor: 4.077

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  11 in total

1.  The evolutionary origin of visual and somatosensory representation in the vertebrate pallium.

Authors:  Shreyas M Suryanarayana; Juan Pérez-Fernández; Brita Robertson; Sten Grillner
Journal:  Nat Ecol Evol       Date:  2020-03-16       Impact factor: 15.460

Review 2.  Orienting our view of the superior colliculus: specializations and general functions.

Authors:  Kathryne M Allen; Jennifer Lawlor; Angeles Salles; Cynthia F Moss
Journal:  Curr Opin Neurobiol       Date:  2021-11-23       Impact factor: 6.627

3.  Bidirectional Control of Orienting Behavior by the Substantia Nigra Pars Reticulata: Distinct Significance of Head and Whisker Movements.

Authors:  Sebastian Hormigo; Ji Zhou; Manuel A Castro-Alamancos
Journal:  eNeuro       Date:  2021-10-21

4.  Layer 5 Corticofugal Projections from Diverse Cortical Areas: Variations on a Pattern of Thalamic and Extrathalamic Targets.

Authors:  Judy A Prasad; Briana J Carroll; S Murray Sherman
Journal:  J Neurosci       Date:  2020-06-12       Impact factor: 6.167

Review 5.  Unraveling circuits of visual perception and cognition through the superior colliculus.

Authors:  Michele A Basso; Martha E Bickford; Jianhua Cang
Journal:  Neuron       Date:  2021-02-05       Impact factor: 17.173

6.  Freely Behaving Mice Can Brake and Turn During Optogenetic Stimulation of the Mesencephalic Locomotor Region.

Authors:  Cornelis Immanuel van der Zouwen; Joël Boutin; Maxime Fougère; Aurélie Flaive; Mélanie Vivancos; Alessandro Santuz; Turgay Akay; Philippe Sarret; Dimitri Ryczko
Journal:  Front Neural Circuits       Date:  2021-04-09       Impact factor: 3.492

Review 7.  The Dopaminergic Control of Movement-Evolutionary Considerations.

Authors:  Juan Pérez-Fernández; Marta Barandela; Cecilia Jiménez-López
Journal:  Int J Mol Sci       Date:  2021-10-19       Impact factor: 5.923

8.  Conserved subcortical processing in visuo-vestibular gaze control.

Authors:  Tobias Wibble; Tony Pansell; Sten Grillner; Juan Pérez-Fernández
Journal:  Nat Commun       Date:  2022-08-10       Impact factor: 17.694

Review 9.  The tectum/superior colliculus as the vertebrate solution for spatial sensory integration and action.

Authors:  Tadashi Isa; Emmanuel Marquez-Legorreta; Sten Grillner; Ethan K Scott
Journal:  Curr Biol       Date:  2021-06-07       Impact factor: 10.900

10.  The neural bases of vertebrate motor behaviour through the lens of evolution.

Authors:  Shreyas M Suryanarayana; Brita Robertson; Sten Grillner
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2021-12-27       Impact factor: 6.237

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