Unraveling circuits of visual perception and cognition through the superior colliculus

Basso, Michele A.; Bickford, Martha E.; Cang, Jianhua

doi:10.1016/j.neuron.2021.01.013

Cited by 146 publications

(153 citation statements)

References 265 publications

(297 reference statements)

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“…In the SC, On-Off DSGC inputs give rise to the direction selectivity of postsynaptic collicular neurons ( Shi et al, 2017 ), indicating that these collicular neurons do not receive retinal inputs from a broad range of RGC types, but specifically from On-Off DSGCs. Since the superficial layer of the SC is well recognized for its roles in encoding spatial locations and instructing stimulus-directed defensive and prey behaviors ( Basso et al, 2021 ; Ito and Feldheim, 2018 ), the encoding of the spatial location of an emerging moving object by On-Off DSGCs may benefit rapid sensorimotor decisions that involve collicular circuitry.…”

Section: Discussionmentioning

confidence: 99%

Spatially displaced excitation contributes to the encoding of interrupted motion by a retinal direction-selective circuit

Ding

Chen

Chung

et al. 2021

eLife

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Spatially distributed excitation and inhibition collectively shape a visual neuron's receptive field (RF) properties. In the direction-selective circuit of the mammalian retina, the role of strong null-direction inhibition of On-Off direction-selective ganglion cells (On-Off DSGCs) on their direction selectivity is well-studied. However, how excitatory inputs influence the On-Off DSGC's visual response is underexplored. Here, we report that On-Off DSGCs have a spatially displaced glutamatergic receptive field along their horizontal preferred-null motion axes. This displaced receptive field contributes to DSGC null-direction spiking during interrupted motion trajectories. Theoretical analyses indicate that population responses during interrupted motion may help populations of On-Off DSGCs signal the spatial location of moving objects in complex, naturalistic visual environments. Our study highlights that the direction-selective circuit exploits separate sets of mechanisms under different stimulus conditions, and these mechanisms may help encode multiple visual features.

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Section: Discussionmentioning

confidence: 99%

Spatially displaced excitation contributes to the encoding of interrupted motion by a retinal direction-selective circuit

Ding

Chen

Chung

et al. 2021

eLife

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“…Finally, we will conclude with perspectives on the key outstanding questions about tectal/SC function, and possible avenues for addressing them. We aim to provide a broad evolutionary perspective on the tectum/SC, its intrinsic circuitry, its interactions with other brain regions, and its contributions to the processing of diverse sensory stimuli, and we refer readers to a very recent and complementary review by Basso et al 18 , which is more focused on the SC's role in vision, especially in mammals including primates. The tectum/SC's position in brainwide networks The retinotectal pathway Retinal ganglion cells, the output neurons of the retina, provide a major input to the tectum/SC in most vertebrates 19 (Figure 1).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2021

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The superior colliculus, or tectum in the case of non-mammalian vertebrates, is a part of the brain that registers events in the surrounding space, often through vision and hearing, but also through electrosensation, infrared detection, and other sensory modalities in diverse vertebrate lineages. This information is used to form maps of the surrounding space and the positions of different salient stimuli in relation to the individual. The sensory maps are arranged in layers with visual input in the uppermost layer, other senses in deeper positions, and a spatially aligned motor map in the deepest layer. Here, we will review the organization and intrinsic function of the tectum/superior colliculus and the information that is processed within tectal circuits. We will also discuss tectal/superior colliculus outputs that are conveyed directly to downstream motor circuits or via the thalamus to cortical areas to control various aspects of behavior. The tectum/superior colliculus is evolutionarily conserved among all vertebrates, but tailored to the sensory specialties of each lineage, and its roles have shifted with the emergence of the cerebral cortex in mammals. We will illustrate both the conserved and divergent properties of the tectum/superior colliculus through vertebrate evolution by comparing tectal processing in lampreys belonging to the oldest group of extant vertebrates, larval zebrafish, rodents, and other vertebrates including primates. ''The tectum/SC's intrinsic networks, and the computations that they perform'', to the sensory and sensorimotor integration ll

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“…This opens up opportunities to investigate how behaviorally relevant visual stimuli in the upper and lower visual field are simultaneously integrated within the SC circuitry and how the activity of the distinct circuits and neuronal populations of the SC relate to behavioral events. In particular, recent studies have indicated that SC plays a more prominent role in higher cognitive functions than previously thought (Basso et al, 2021). Combining the tangential recording approach with modern and sophisticated behavioral paradigms in mice has the potential to significantly advance our understanding on the role of SC during behavior.…”

Section: Discussionmentioning

confidence: 99%

“…While the SC has been studied extensively on the single neuron level (Ahmadlou and Heimel, 2015; Ahmadlou et al, 2017; Gale and Murphy, 2018; 2016; 2014; Inayat et al, 2015; Lee et al, 2020; Shi et al, 2017; L. Wang et al, 2010), the role of its neural circuits and specific cell-types under in vivo conditions, in awake behaving animals, remains elusive. Recently, its role in sensory processing and also its participation in higher cognitive functions regained attention because modern genetic tools and sophisticated behavioral measurements became available (Basso and May, 2017; Zhao et al, 2014; Basso et al, 2021; Cang et al, 2018; De Franceschi and Solomon, 2018; Evans et al, 2018; Ito and Feldheim, 2018; Reinhard et al, 2019; Sans-Dublanc et al, 2021; Savier et al, 2019; Villalobos et al, 2018; Zhang et al, 2019). However, it is still not well understood how sensory information from the complex and dynamic visual environment of the entire visual field (Qiu, et al, 2021) is represented at the population level within SC and what role the different cell-types play in extracting and representing behaviorally relevant information (Gale and Murphy, 2014; Hoy et al, 2019; Sans-Dublanc et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Tangential high-density electrode insertions allow to simultaneously measure neuronal activity across an extended region of the visual field in mouse superior colliculus

Sibille

Gehr

Teh

et al. 2021

Preprint

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The superior colliculus (SC) is a midbrain structure that plays a central role in visual processing. Although we have learned a considerable amount about the function of single SC neurons, the way in which sensory information is represented and processed on the population level in awake behaving animals and across a large region of the retinotopic map is still largely unknown. Partially because the SC is anatomically located below the cortical sheet and the transverse sinus, it is technically difficult to measure neuronal activity from a large population of neurons in SC. To address this, we propose a tangential recording configuration using high-density electrode probes (Neuropixels) in mouse SC in vivo that permits a large number of recording sites (~200) accessibility inside the SC circuitry. This approach thereby provides a unique opportunity to measure the activity of SC neuronal populations composing up to ~2 mm of SC tissue and characterized by receptive fields covering an extended region in the visual field. Here we describe how to perform tangential recordings along the anterior-posterior and the medio-lateral axis of the mouse SC in vivo and how to combine this approach with optogenetic tools for cell-type identification on the population level.

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Unraveling circuits of visual perception and cognition through the superior colliculus

Cited by 146 publications

References 265 publications

Spatially displaced excitation contributes to the encoding of interrupted motion by a retinal direction-selective circuit

Spatially displaced excitation contributes to the encoding of interrupted motion by a retinal direction-selective circuit

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

Tangential high-density electrode insertions allow to simultaneously measure neuronal activity across an extended region of the visual field in mouse superior colliculus

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