Editorial

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Open AccessEditorial

Molecular Mechanisms of Neural Plasticity: From Basic Research to Implications for Visual Functional Rescue

by Alessandro Sale

Int. J. Mol. Sci. 2022, 23(21), 13183; https://doi.org/10.3390/ijms232113183 - 29 Oct 2022

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Visual system plasticity, the capability of visual connections to modify their structure and function in response to experience, is an essential property underlying the maturation of visual functions during development, behavioral flexibility in response to subtle environmental changes, and adaptive repair in conditions [...] Read more.

Visual system plasticity, the capability of visual connections to modify their structure and function in response to experience, is an essential property underlying the maturation of visual functions during development, behavioral flexibility in response to subtle environmental changes, and adaptive repair in conditions of disease or trauma [...] Full article

(This article belongs to the Special Issue Molecular Mechanisms of Neural Plasticity: From Basic Research to Implications for Visual Functional Rescue)

Research

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16 pages, 1961 KiB

Open AccessCommunication

High-Contrast Stimulation Potentiates the Neurotrophic Properties of Müller Cells and Suppresses Their Pro-Inflammatory Phenotype

by Miloslav Zloh, Patrik Kutilek and Andrea Stofkova

Int. J. Mol. Sci. 2022, 23(15), 8615; https://doi.org/10.3390/ijms23158615 - 03 Aug 2022

Cited by 1 | Viewed by 1846

Abstract

High-contrast visual stimulation promotes retinal regeneration and visual function, but the underlying mechanism is not fully understood. Here, we hypothesized that Müller cells (MCs), which express neurotrophins such as brain-derived neurotrophic factor (BDNF), could be key players in this retinal plasticity process. This [...] Read more.

High-contrast visual stimulation promotes retinal regeneration and visual function, but the underlying mechanism is not fully understood. Here, we hypothesized that Müller cells (MCs), which express neurotrophins such as brain-derived neurotrophic factor (BDNF), could be key players in this retinal plasticity process. This hypothesis was tested by conducting in vivo and in vitro high-contrast stimulation of adult mice and MCs. Following stimulation, we examined the expression of BDNF and its inducible factor, VGF, in the retina and MCs. We also investigated the alterations in the expression of VGF, nuclear factor kappa B (NF-κB) and pro-inflammatory mediators in MCs, as well as their capacity to proliferate and develop a neurogenic or reactive gliosis phenotype after high-contrast stimulation and treatment with BDNF. Our results showed that high-contrast stimulation upregulated BDNF levels in MCs in vivo and in vitro. The additional BDNF treatment significantly augmented VGF production in MCs and their neuroprotective features, as evidenced by increased MC proliferation, neurodifferentiation, and decreased expression of the pro-inflammatory factors and the reactive gliosis marker GFAP. These results demonstrate that high-contrast stimulation activates the neurotrophic and neuroprotective properties of MCs, suggesting their possible direct involvement in retinal neuronal survival and improved functional outcomes in response to visual stimulation. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Neural Plasticity: From Basic Research to Implications for Visual Functional Rescue)

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21 pages, 3429 KiB

Open AccessArticle

Chronic Monocular Deprivation Reveals MMP9-Dependent and -Independent Aspects of Murine Visual System Plasticity

by Sachiko Murase, Sarah E. Robertson, Crystal L. Lantz, Ji Liu, Daniel E. Winkowski and Elizabeth M. Quinlan

Int. J. Mol. Sci. 2022, 23(5), 2438; https://doi.org/10.3390/ijms23052438 - 23 Feb 2022

Cited by 3 | Viewed by 2203

Abstract

The deletion of matrix metalloproteinase MMP9 is combined here with chronic monocular deprivation (cMD) to identify the contributions of this proteinase to plasticity in the visual system. Calcium imaging of supragranular neurons of the binocular region of primary visual cortex (V1b) of wild-type [...] Read more.

The deletion of matrix metalloproteinase MMP9 is combined here with chronic monocular deprivation (cMD) to identify the contributions of this proteinase to plasticity in the visual system. Calcium imaging of supragranular neurons of the binocular region of primary visual cortex (V1b) of wild-type mice revealed that cMD initiated at eye opening significantly decreased the strength of deprived-eye visual responses to all stimulus contrasts and spatial frequencies. cMD did not change the selectivity of V1b neurons for the spatial frequency, but orientation selectivity was higher in low spatial frequency-tuned neurons, and orientation and direction selectivity were lower in high spatial frequency-tuned neurons. Constitutive deletion of MMP9 did not impact the stimulus selectivity of V1b neurons, including ocular preference and tuning for spatial frequency, orientation, and direction. However, MMP9^−/− mice were completely insensitive to plasticity engaged by cMD, such that the strength of the visual responses evoked by deprived-eye stimulation was maintained across all stimulus contrasts, orientations, directions, and spatial frequencies. Other forms of experience-dependent plasticity, including stimulus selective response potentiation, were normal in MMP9^−/− mice. Thus, MMP9 activity is dispensable for many forms of activity-dependent plasticity in the mouse visual system, but is obligatory for the plasticity engaged by cMD. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Neural Plasticity: From Basic Research to Implications for Visual Functional Rescue)

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17 pages, 19280 KiB

Open AccessArticle

Manipulating the Level of Sensorimotor Stimulation during LI-rTMS Can Improve Visual Circuit Reorganisation in Adult Ephrin-A2A5^-/- Mice

by Eugenia Z. Poh, Courtney Green, Luca Agostinelli, Marissa Penrose-Menz, Ann-Kathrin Karl, Alan R. Harvey and Jennifer Rodger

Int. J. Mol. Sci. 2022, 23(5), 2418; https://doi.org/10.3390/ijms23052418 - 22 Feb 2022

Cited by 4 | Viewed by 2095

Abstract

Repetitive transcranial magnetic stimulation (rTMS) is a non-invasive brain stimulation technique that has the potential to treat a variety of neurologic and psychiatric disorders. The extent of rTMS-induced neuroplasticity may be dependent on a subject’s brain state at the time of stimulation. Chronic [...] Read more.

Repetitive transcranial magnetic stimulation (rTMS) is a non-invasive brain stimulation technique that has the potential to treat a variety of neurologic and psychiatric disorders. The extent of rTMS-induced neuroplasticity may be dependent on a subject’s brain state at the time of stimulation. Chronic low intensity rTMS (LI-rTMS) has previously been shown to induce beneficial structural and functional reorganisation within the abnormal visual circuits of ephrin-A2A5^-/- mice in ambient lighting. Here, we administered chronic LI-rTMS in adult ephrin-A2A5^-/- mice either in a dark environment or concurrently with voluntary locomotion. One day after the last stimulation session, optokinetic responses were assessed and fluorescent tracers were injected to map corticotectal and geniculocortical projections. We found that LI-rTMS in either treatment condition refined the geniculocortical map. Corticotectal projections were improved in locomotion+LI-rTMS subjects, but not in dark + LI-rTMS and sham groups. Visuomotor behaviour was not improved in any condition. Our results suggest that the beneficial reorganisation of abnormal visual circuits by rTMS can be significantly influenced by simultaneous, ambient visual input and is enhanced by concomitant physical exercise. Furthermore, the observed pathway-specific effects suggest that regional molecular changes and/or the relative proximity of terminals to the induced electric fields influence the outcomes of LI-rTMS on abnormal circuitry. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Neural Plasticity: From Basic Research to Implications for Visual Functional Rescue)

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34 pages, 41113 KiB

Open AccessArticle

Depletion of Retinal Dopaminergic Activity in a Mouse Model of Rod Dysfunction Exacerbates Experimental Autoimmune Uveoretinitis: A Role for the Gateway Reflex

by Andrea Stofkova, Miloslav Zloh, Dominika Andreanska, Ivana Fiserova, Jan Kubovciak, Jan Hejda, Patrik Kutilek and Masaaki Murakami

Int. J. Mol. Sci. 2022, 23(1), 453; https://doi.org/10.3390/ijms23010453 - 31 Dec 2021

Cited by 4 | Viewed by 3360

Abstract

The gateway reflex is a mechanism by which neural inputs regulate chemokine expression at endothelial cell barriers, thereby establishing gateways for the invasion of autoreactive T cells into barrier-protected tissues. In this study, we hypothesized that rod photoreceptor dysfunction causes remodeling of retinal [...] Read more.

The gateway reflex is a mechanism by which neural inputs regulate chemokine expression at endothelial cell barriers, thereby establishing gateways for the invasion of autoreactive T cells into barrier-protected tissues. In this study, we hypothesized that rod photoreceptor dysfunction causes remodeling of retinal neural activity, which influences the blood–retinal barrier and the development of retinal inflammation. We evaluated this hypothesis using Gnat1^rd17 mice, a model of night blindness with late-onset rod-cone dystrophy, and experimental autoimmune uveoretinitis (EAU). Retinal remodeling and its effect on EAU development were investigated by transcriptome profiling, target identification, and functional validation. We showed that Gnat1^rd17 mice primarily underwent alterations in their retinal dopaminergic system, triggering the development of an exacerbated EAU, which was counteracted by dopamine replacement with L-DOPA administered either systemically or locally. Remarkably, dopamine acted on retinal endothelial cells to inhibit NF-κB and STAT3 activity and the expression of downstream target genes such as chemokines involved in T cell recruitment. These results suggest that rod-mediated dopamine release functions in a gateway reflex manner in the homeostatic control of immune cell entry into the retina, and the loss of retinal dopaminergic activity in conditions associated with rod dysfunction increases the susceptibility to autoimmune uveitis. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Neural Plasticity: From Basic Research to Implications for Visual Functional Rescue)

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Graphical abstract

14 pages, 1281 KiB

Open AccessArticle

Visual Cortex Engagement in Retinitis Pigmentosa

by Gianluca Pietra, Tiziana Bonifacino, Davide Talamonti, Giambattista Bonanno, Alessandro Sale, Lucia Galli and Laura Baroncelli

Int. J. Mol. Sci. 2021, 22(17), 9412; https://doi.org/10.3390/ijms22179412 - 30 Aug 2021

Cited by 5 | Viewed by 2475

Abstract

Retinitis pigmentosa (RP) is a family of inherited disorders caused by the progressive degeneration of retinal photoreceptors. There is no cure for RP, but recent research advances have provided promising results from many clinical trials. All these therapeutic strategies are focused on preserving [...] Read more.

Retinitis pigmentosa (RP) is a family of inherited disorders caused by the progressive degeneration of retinal photoreceptors. There is no cure for RP, but recent research advances have provided promising results from many clinical trials. All these therapeutic strategies are focused on preserving existing photoreceptors or substituting light-responsive elements. Vision recovery, however, strongly relies on the anatomical and functional integrity of the visual system beyond photoreceptors. Although the retinal structure and optic pathway are substantially preserved at least in early stages of RP, studies describing the visual cortex status are missing. Using a well-established mouse model of RP, we analyzed the response of visual cortical circuits to the progressive degeneration of photoreceptors. We demonstrated that the visual cortex goes through a transient and previously undescribed alteration in the local excitation/inhibition balance, with a net shift towards increased intracortical inhibition leading to improved filtering and decoding of corrupted visual inputs. These results suggest a compensatory action of the visual cortex that increases the range of residual visual sensitivity in RP. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Neural Plasticity: From Basic Research to Implications for Visual Functional Rescue)

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Review

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15 pages, 2136 KiB

Open AccessReview

Retinal Plasticity

by Enrica Strettoi, Beatrice Di Marco, Noemi Orsini and Debora Napoli

Int. J. Mol. Sci. 2022, 23(3), 1138; https://doi.org/10.3390/ijms23031138 - 20 Jan 2022

Cited by 9 | Viewed by 2367

Abstract

Brain plasticity is a well-established concept designating the ability of central nervous system (CNS) neurons to rearrange as a result of learning, when adapting to changeable environmental conditions or else while reacting to injurious factors. As a part of the CNS, the retina [...] Read more.

Brain plasticity is a well-established concept designating the ability of central nervous system (CNS) neurons to rearrange as a result of learning, when adapting to changeable environmental conditions or else while reacting to injurious factors. As a part of the CNS, the retina has been repeatedly probed for its possible ability to respond plastically to a variably altered environment or to pathological insults. However, numerous studies support the conclusion that the retina, outside the developmental stage, is endowed with only limited plasticity, exhibiting, instead, a remarkable ability to maintain a stable architectural and functional organization. Reviewed here are representative examples of hippocampal and cortical paradigms of plasticity and of retinal structural rearrangements found in organization and circuitry following altered developmental conditions or occurrence of genetic diseases leading to neuronal degeneration. The variable rate of plastic changes found in mammalian retinal neurons in different circumstances is discussed, focusing on structural plasticity. The likely adaptive value of maintaining a low level of plasticity in an organ subserving a sensory modality that is dominant for the human species and that requires elevated fidelity is discussed. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Neural Plasticity: From Basic Research to Implications for Visual Functional Rescue)

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Other

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14 pages, 2416 KiB

Open AccessCase Report

Normal Retinotopy in Primary Visual Cortex in a Congenital Complete Unilateral Lesion of Lateral Geniculate Nucleus in Human: A Case Study

by Akshatha Bhat, Jan W. Kurzawski, Giovanni Anobile, Francesca Tinelli, Laura Biagi and Maria Concetta Morrone

Int. J. Mol. Sci. 2022, 23(3), 1055; https://doi.org/10.3390/ijms23031055 - 19 Jan 2022

Cited by 2 | Viewed by 2417

Abstract

Impairment of the geniculostriate pathway results in scotomas in the corresponding part of the visual field. Here, we present a case of patient IB with left eye microphthalmia and with lesions in most of the left geniculostriate pathway, including the Lateral Geniculate Nucleus [...] Read more.

Impairment of the geniculostriate pathway results in scotomas in the corresponding part of the visual field. Here, we present a case of patient IB with left eye microphthalmia and with lesions in most of the left geniculostriate pathway, including the Lateral Geniculate Nucleus (LGN). Despite the severe lesions, the patient has a very narrow scotoma in the peripheral part of the lower-right-hemifield only (beyond 15° of eccentricity) and complete visual field representation in the primary visual cortex. Population receptive field mapping (pRF) of the patient’s visual field reveals orderly eccentricity maps together with contralateral activation in both hemispheres. With diffusion tractography, we revealed connections between superior colliculus (SC) and cortical structures in the hemisphere affected by the lesions, which could mediate the retinotopic reorganization at the cortical level. Our results indicate an astonishing case for the flexibility of the developing retinotopic maps where the contralateral thalamus receives fibers from both the nasal and temporal retinae. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Neural Plasticity: From Basic Research to Implications for Visual Functional Rescue)

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