Dataset Information

Rod-cone signal interference in the retina shapes perception in primates.

ABSTRACT: Linking the activity of neurons, circuits and synapses to human behavior is a fundamental goal of neuroscience. Meeting this goal is challenging, in part because behavior, particularly perception, often masks the complexity of the underlying neural circuits, and in part because of the significant behavioral differences between primates and animals like mice and flies in which genetic manipulations are relatively common. Here we relate circuit-level processing of rod and cone signals in the non-human primate retina to a known break in the normal seamlessness of human vision - a surprising inability to see high contrast flickering lights under specific conditions. We use electrophysiological recordings and perceptual experiments to identify key mechanisms that shape the retinal integration of rod- and cone-generated retinal signals. We then incorporate these mechanistic insights into a predicti\ve model that accurately captures the cancellation of rod- and cone-mediated responses and can explain the perceptual insensitivity to flicker.

SUBMITTER: Songco-Aguas A

PROVIDER: S-EPMC11182321 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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Rod-cone signal interference in the retina shapes perception in primates.

Songco-Aguas Adree A Grimes William N WN Rieke Fred F

Frontiers in ophthalmology 20230731

Linking the activity of neurons, circuits and synapses to human behavior is a fundamental goal of neuroscience. Meeting this goal is challenging, in part because behavior, particularly perception, often masks the complexity of the underlying neural circuits, and in part because of the significant behavioral differences between primates and animals like mice and flies in which genetic manipulations are relatively common. Here we relate circuit-level processing of rod and cone signals in the non-h ...[more]

PMID: 38983027

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Project description:Cone rod dystrophies (CRDs) (prevalence 1/40,000) are inherited retinal dystrophies that belong to the group of pigmentary retinopathies. CRDs are characterized by retinal pigment deposits visible on fundus examination, predominantly localized to the macular region. In contrast to typical retinitis pigmentosa (RP), also called the rod cone dystrophies (RCDs) resulting from the primary loss in rod photoreceptors and later followed by the secondary loss in cone photoreceptors, CRDs reflect the opposite sequence of events. CRD is characterized by primary cone involvement, or, sometimes, by concomitant loss of both cones and rods that explains the predominant symptoms of CRDs: decreased visual acuity, color vision defects, photoaversion and decreased sensitivity in the central visual field, later followed by progressive loss in peripheral vision and night blindness. The clinical course of CRDs is generally more severe and rapid than that of RCDs, leading to earlier legal blindness and disability. At end stage, however, CRDs do not differ from RCDs. CRDs are most frequently non syndromic, but they may also be part of several syndromes, such as Bardet Biedl syndrome and Spinocerebellar Ataxia Type 7 (SCA7). Non syndromic CRDs are genetically heterogeneous (ten cloned genes and three loci have been identified so far). The four major causative genes involved in the pathogenesis of CRDs are ABCA4 (which causes Stargardt disease and also 30 to 60% of autosomal recessive CRDs), CRX and GUCY2D (which are responsible for many reported cases of autosomal dominant CRDs), and RPGR (which causes about 2/3 of X-linked RP and also an undetermined percentage of X-linked CRDs). It is likely that highly deleterious mutations in genes that otherwise cause RP or macular dystrophy may also lead to CRDs. The diagnosis of CRDs is based on clinical history, fundus examination and electroretinogram. Molecular diagnosis can be made for some genes, genetic counseling is always advised. Currently, there is no therapy that stops the evolution of the disease or restores the vision, and the visual prognosis is poor. Management aims at slowing down the degenerative process, treating the complications and helping patients to cope with the social and psychological impact of blindness.

Project description:Key pointsAlthough cone and rod photoreceptor cells in the retina have a type of cannabinoid receptor called a CB1 receptor, little is known about how cannabinoids, the active component in marijuana, affect retinal function. Studies have shown that a circadian (24-h) clock in the retina uses dopamine receptors, which are also on photoreceptors, to regulate gap junctions (a type of cell-to-cell communication) between rods and cones, so that they are functional (open) at night but closed in the day. We show that CB1 receptors have opposite effects on rod-cone gap junctions in day and night, decreasing communication in the day when dopamine receptors are active and increasing communication when dopamine receptors are inactive. CB1 and dopamine receptors thus work together to enhance the day/night difference in rod-cone gap junction communication. The increased rod-cone communication at night due to cannabinoid CB1 receptors may help improve night vision.AbstractCannabinoid CB1 receptors and dopamine D4 receptors in the brain form receptor complexes that interact but the physiological function of these interactions in intact tissue remains unclear. In vertebrate retina, rods and cones, which are connected by gap junctions, express both CB1 and D4 receptors. Because the retinal circadian clock uses cone D4 receptors to decrease rod-cone gap junction coupling in the day and to increase it at night, we studied whether an interaction between cone CB1 and D4 receptors increases the day/night difference in rod-cone coupling compared to D4 receptors acting alone. Using electrical recording and injections of Neurobiotin tracer into individual cones in intact goldfish retinas, we found that SR141716A (a CB1 receptor antagonist) application alone in the day increased both the extent of rod-cone tracer coupling and rod input to cones, which reaches cones via open gap junctions. Conversely, SR141716A application alone at night or SR141716A application in the day following 30-min spiperone (a D4 receptor antagonist) application decreased both rod-cone tracer coupling and rod input to cones. These results show that endogenous activation of cone CB1 receptors decreases rod-cone coupling in the day when D4 receptors are activated but increases it at night when D4 receptors are not activated. Therefore, the D4 receptor-dependent day/night switch in the effects of CB1 receptor activation results in an enhancement of the day/night difference in rod-cone coupling. This synergistic interaction increases detection of very dim large objects at night and fine spatial details in the day.

Dataset Information

Rod-cone signal interference in the retina shapes perception in primates.

Publications

Rod-cone signal interference in the retina shapes perception in primates.

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