Dataset Information

Vision Changes the Cellular Composition of Binocular Circuitry during the Critical Period.

ABSTRACT: High acuity stereopsis emerges during an early postnatal critical period when binocular neurons in the primary visual cortex sharpen their receptive field tuning properties. We find that this sharpening is achieved by dismantling the binocular circuit present at critical period onset and building it anew. Longitudinal imaging of receptive field tuning (e.g., orientation selectivity) of thousands of neurons reveals that most binocular neurons present in layer 2/3 at critical period onset are poorly tuned and are rendered monocular. In parallel, new binocular neurons are established by conversion of well-tuned monocular neurons as they gain matched input from the other eye. These improvements in binocular tuning in layer 2/3 are not inherited from layer 4 but are driven by the experience-dependent sharpening of ipsilateral eye responses. Thus, vision builds a new and more sharply tuned binocular circuit in layer 2/3 by cellular exchange and not by refining the original circuit.

SUBMITTER: Tan L

PROVIDER: S-EPMC7704707 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Vision Changes the Cellular Composition of Binocular Circuitry during the Critical Period.

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

Neuron 20201021 4

High acuity stereopsis emerges during an early postnatal critical period when binocular neurons in the primary visual cortex sharpen their receptive field tuning properties. We find that this sharpening is achieved by dismantling the binocular circuit present at critical period onset and building it anew. Longitudinal imaging of receptive field tuning (e.g., orientation selectivity) of thousands of neurons reveals that most binocular neurons present in layer 2/3 at critical period onset are poor ...[more]

PMID: 33091339

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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 Changes the Cellular Composition of Binocular Circuitry during the Critical Period.

Publications

Vision Changes the Cellular Composition of Binocular Circuitry during the Critical Period.

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