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      The Superior Colliculus: Cell Types, Connectivity, and Behavior

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          Abstract

          The superior colliculus (SC), one of the most well-characterized midbrain sensorimotor structures where visual, auditory, and somatosensory information are integrated to initiate motor commands, is highly conserved across vertebrate evolution. Moreover, cell-type-specific SC neurons integrate afferent signals within local networks to generate defined output related to innate and cognitive behaviors. This review focuses on the recent progress in understanding of phenotypic diversity amongst SC neurons and their intrinsic circuits and long-projection targets. We further describe relevant neural circuits and specific cell types in relation to behavioral outputs and cognitive functions. The systematic delineation of SC organization, cell types, and neural connections is further put into context across species as these depend upon laminar architecture. Moreover, we focus on SC neural circuitry involving saccadic eye movement, and cognitive and innate behaviors. Overall, the review provides insight into SC functioning and represents a basis for further understanding of the pathology associated with SC dysfunction.

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          Most cited references234

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          Spatial Transcriptomics and In Situ Sequencing to Study Alzheimer’s Disease

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            AAV-Mediated Anterograde Transsynaptic Tagging: Mapping Corticocollicular Input-Defined Neural Pathways for Defense Behaviors.

            To decipher neural circuits underlying brain functions, viral tracers are widely applied to map input and output connectivity of neuronal populations. Despite the successful application of retrograde transsynaptic viruses for identifying presynaptic neurons of transduced neurons, analogous anterograde transsynaptic tools for tagging postsynaptically targeted neurons remain under development. Here, we discovered that adeno-associated viruses (AAV1 and AAV9) exhibit anterograde transsynaptic spread properties. AAV1-Cre from transduced presynaptic neurons effectively and specifically drives Cre-dependent transgene expression in selected postsynaptic neuronal targets, thus allowing axonal tracing and functional manipulations of the latter input-defined neuronal population. Its application in superior colliculus (SC) reveals that SC neuron subpopulations receiving corticocollicular projections from auditory and visual cortex specifically drive flight and freezing, two different types of defense behavior, respectively. Together with an intersectional approach, AAV-mediated anterograde transsynaptic tagging can categorize neurons by their inputs and molecular identity, and allow forward screening of distinct functional neural pathways embedded in complex brain circuits.
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              Rapid innate defensive responses of mice to looming visual stimuli.

              Much of brain science is concerned with understanding the neural circuits that underlie specific behaviors. While the mouse has become a favorite experimental subject, the behaviors of this species are still poorly explored. For example, the mouse retina, like that of other mammals, contains ∼20 different circuits that compute distinct features of the visual scene [1, 2]. By comparison, only a handful of innate visual behaviors are known in this species--the pupil reflex [3], phototaxis [4], the optomotor response [5], and the cliff response [6]--two of which are simple reflexes that require little visual processing. We explored the behavior of mice under a visual display that simulates an approaching object, which causes defensive reactions in some other species [7, 8]. We show that mice respond to this stimulus either by initiating escape within a second or by freezing for an extended period. The probability of these defensive behaviors is strongly dependent on the parameters of the visual stimulus. Directed experiments identify candidate retinal circuits underlying the behavior and lead the way into detailed study of these neural pathways. This response is a new addition to the repertoire of innate defensive behaviors in the mouse that allows the detection and avoidance of aerial predators.
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                Author and article information

                Contributors
                lp.wang@siat.ac.cn
                feng.wang@siat.ac.cn
                Journal
                Neurosci Bull
                Neurosci Bull
                Neuroscience Bulletin
                Springer Nature Singapore (Singapore )
                1673-7067
                1995-8218
                28 April 2022
                28 April 2022
                December 2022
                : 38
                : 12
                : 1519-1540
                Affiliations
                [1 ]GRID grid.458489.c, ISNI 0000 0001 0483 7922, Shenzhen Key Lab of Neuropsychiatric Modulation, Guangdong Provincial Key Laboratory of Brain Connectome and Behavior, CAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, ; Shenzhen, 518055 China
                [2 ]GRID grid.410726.6, ISNI 0000 0004 1797 8419, University of Chinese Academy of Sciences, ; Beijing, 100049 China
                [3 ]GRID grid.17091.3e, ISNI 0000 0001 2288 9830, Michael Smith Laboratories and Djavad Mowafaghian Centre for Brain Health, , University of British Columbia, ; Vancouver, V6T 1Z4 Canada
                [4 ]GRID grid.410717.4, ISNI 0000 0004 0644 5086, National Institute of Biological Sciences, ; Beijing, 100049 China
                Article
                858
                10.1007/s12264-022-00858-1
                9723059
                35484472
                2a24ffeb-18f2-44fc-bc0b-74aa440d18b9
                © The Author(s) 2022

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 29 December 2021
                : 16 February 2022
                Categories
                Review
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                © Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences 2022

                superior colliculus,glutamatergic neurons,gabaergic neurons,neuronal circuits,innate behaviors

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