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Vision is required for the formation of binocular neurons prior to the classical critical period.

ABSTRACT: Depth perception emerges from the development of binocular neurons in primary visual cortex. Vision is required for these neurons to acquire their mature responses to visual stimuli. The prevailing view is that vision does not influence binocular circuitry until the onset of the critical period, about a week after eye opening, and that plasticity of visual responses is triggered by increased inhibition. Here, we show that vision is required to form binocular neurons and to improve binocular tuning and matching from eye opening until critical period closure. Enhancing inhibition does not accelerate this process. Vision soon after eye opening improves the tuning properties of binocular neurons by strengthening and sharpening ipsilateral eye cortical responses. This progressively changes the population of neurons in the binocular pool, and this plasticity is sensitive to interocular differences prior to critical period onset. Thus, vision establishes binocular circuitry and guides binocular plasticity from eye opening.

SUBMITTER: Tan L

PROVIDER: S-EPMC8511080 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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Vision is required for the formation of binocular neurons prior to the classical critical period.

Tan Liming L Ringach Dario L DL Zipursky S Lawrence SL Trachtenberg Joshua T JT

Current biology : CB 20210818 19

Depth perception emerges from the development of binocular neurons in primary visual cortex. Vision is required for these neurons to acquire their mature responses to visual stimuli. The prevailing view is that vision does not influence binocular circuitry until the onset of the critical period, about a week after eye opening, and that plasticity of visual responses is triggered by increased inhibition. Here, we show that vision is required to form binocular neurons and to improve binocular tuni ...[more]

PMID: 34411526

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Project description:Study of the neural deficits caused by mismatched binocular vision in early childhood has predominantly focused on circuits in the primary visual cortex (V1). Recent evidence has revealed that neurons in mouse dorsolateral geniculate nucleus (dLGN) can undergo rapid ocular dominance plasticity following monocular deprivation (MD). It remains unclear, however, whether the long-lasting deficits attributed to MD during the critical period originate in the thalamus. Using in vivo two-photon Ca2+ imaging of dLGN afferents in superficial layers of V1 in female and male mice, we demonstrate that 14 d MD during the critical period leads to a chronic loss of binocular dLGN inputs while sparing response strength and spatial acuity. Importantly, MD leads to profoundly mismatched visual tuning properties in remaining binocular dLGN afferents. Furthermore, MD impairs binocular modulation, reducing facilitation of responses of both binocular and monocular dLGN inputs during binocular viewing. As predicted by our findings in thalamic inputs, Ca2+ imaging from V1 neurons revealed spared spatial acuity but impaired binocularity in L4 neurons. V1 L2/3 neurons in contrast displayed deficits in both binocularity and spatial acuity. Our data demonstrate that critical-period MD produces long-lasting disruptions in binocular integration beginning in early binocular circuits in dLGN, whereas spatial acuity deficits first arise from circuits further downstream in V1. Our findings indicate that the development of normal binocular vision and spatial acuity depend upon experience-dependent refinement of distinct stages in the mammalian visual system.SIGNIFICANCE STATEMENT Abnormal binocular vision and reduced acuity are hallmarks of amblyopia, a disorder that affects 2%-5% of the population. It is widely thought that the neural deficits underlying amblyopia begin in the circuits of primary visual cortex. Using in vivo two-photon calcium imaging of thalamocortical axons in mice, we show that depriving one eye of input during a critical period in development chronically impairs binocular integration in thalamic inputs to primary visual cortex. In contrast, visual acuity is spared in thalamic inputs. These findings shed new light on the role for developmental mechanisms in the thalamus in establishing binocular vision and may have critical implications for amblyopia.

Dataset Information

Vision is required for the formation of binocular neurons prior to the classical critical period.

Publications

Vision is required for the formation of binocular neurons prior to the classical critical period.

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