Visual experience-dependent development of ocular dominance columns in pigmented rats

Zhou, Qing; Li, Hangqi; Yao, Songping; Takahata, Toru

doi:10.1093/cercor/bhad196

Cited by 3 publications

(1 citation statement)

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“…For instance, there is a distinction between dorsal and ventral visual pathways both anatomically and physiologically in rodents (Murakami et al, 2017 ). Ocular dominance columns (ODCs), once thought to be unique to primates and carnivores, have been discovered in rats, and their developmental events appear similar to those in primate/carnivore ODCs (Zhou et al, 2023 ). Thus, rodent brains can be considered prototypes of primate brains, despite lacking a prominent fovea.…”

Section: Discussionmentioning

confidence: 99%

Topographic organization across foveal visual areas in macaques

Li,

Hu,

Tanigawa

et al. 2024

Front. Neuroanat.

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IntroductionWhile the fovea on the retina covers only a small region of the visual field, a significant portion of the visual cortex is dedicated to processing information from the fovea being a critical center for object recognition, motion control, and visually guided attention. Despite its importance, prior functional imaging studies in awake monkeys often focused on the parafoveal visual field, potentially leading to inaccuracies in understanding the brain structure underlying function.MethodsIn this study, our aim is to unveil the neuronal connectivity and topography in the foveal visual cortex in comparison to the parafoveal visual cortex. Using four different types of retrograde tracers, we selectively injected them into the striate cortex (V1) or V4, encompassing the regions between the fovea and parafovea.ResultsV1 and V4 exhibited intense mutual connectivity in the foveal visual field, in contrast to the parafoveal visual field, possibly due to the absence of V3 in the foveal visual field. While previous live brain imaging studies failed to reveal retinotopy in the foveal visual fields, our results indicate that the foveal visual fields have continuous topographic connectivity across V1 through V4, as well as the parafoveal visual fields. Although a simple extension of the retinotopic isoeccentricity maps from V1 to V4 has been suggested from previous fMRI studies, our study demonstrated that V3 and V4 possess gradually smaller topographic maps compared to V1 and V2. Feedback projections to foveal V1 primarily originate from the infragranular layers of foveal V2 and V4, while feedforward projections to foveal V4 arise from both supragranular and infragranular layers of foveal V1 and V2, consistent with previous findings in the parafoveal visual fields.DiscussionThis study provides valuable insights into the connectivity of the foveal visual cortex, which was ambiguous in previous imaging studies.

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Section: Discussionmentioning

confidence: 99%

Topographic organization across foveal visual areas in macaques

Li,

Hu,

Tanigawa

et al. 2024

Front. Neuroanat.

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Three-dimensional topography of eye-specific domains in the lateral geniculate nucleus of pigmented and albino rats

Zhou

Chen

et al. 2023

Cerebral Cortex

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We previously revealed the presence of ocular dominance columns (ODCs) in the primary visual cortex (V1) of pigmented rats. On the other hand, previous studies have shown that the ipsilateral-eye domains of the dorsal lateral geniculate nucleus (dLGN) are segregated into a handful of patches in pigmented rats. To investigate the three-dimensional (3D) topography of the eye-specific patches of the dLGN and its relationship with ODCs, we injected different tracers into the right and left eyes and examined strain difference, development, and plasticity of the patches. Furthermore, we applied the tissue clearing technique to reveal the 3D morphology of the LGN and were able to observe entire retinotopic map of the rat dLGN at a certain angle. Our results show that the ipsilateral domains of the dLGN appear mesh-like at any angle and are developed at around time of eye-opening. Their development was moderately affected by abnormal visual experience, but the patch formation was not disrupted. In albino Wistar rats, ipsilateral patches were observed in the dLGN, but they were much fewer, especially near the central visual field. These results provide insights into how ipsilateral patches of the dLGN arise, and how the geniculo-cortical arrangement is different between rodents and primates.

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Development of ocular dominance columns across rodents and other species: revisiting the concept of critical period plasticity

Takahata

2024

Front. Neural Circuits

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The existence of cortical columns, regarded as computational units underlying both lower and higher-order information processing, has long been associated with highly evolved brains, and previous studies suggested their absence in rodents. However, recent discoveries have unveiled the presence of ocular dominance columns (ODCs) in the primary visual cortex (V1) of Long-Evans rats. These domains exhibit continuity from layer 2 through layer 6, confirming their identity as genuine ODCs. Notably, ODCs are also observed in Brown Norway rats, a strain closely related to wild rats, suggesting the physiological relevance of ODCs in natural survival contexts, although they are lacking in albino rats. This discovery has enabled researchers to explore the development and plasticity of cortical columns using a multidisciplinary approach, leveraging studies involving hundreds of individuals—an endeavor challenging in carnivore and primate species. Notably, developmental trajectories differ depending on the aspect under examination: while the distribution of geniculo-cortical afferent terminals indicates matured ODCs even before eye-opening, consistent with prevailing theories in carnivore/primate studies, examination of cortical neuron spiking activities reveals immature ODCs until postnatal day 35, suggesting delayed maturation of functional synapses which is dependent on visual experience. This developmental gap might be recognized as ‘critical period’ for ocular dominance plasticity in previous studies. In this article, I summarize cross-species differences in ODCs and geniculo-cortical network, followed by a discussion on the development, plasticity, and evolutionary significance of rat ODCs. I discuss classical and recent studies on critical period plasticity in the venue where critical period plasticity might be a component of experience-dependent development. Consequently, this series of studies prompts a paradigm shift in our understanding of species conservation of cortical columns and the nature of plasticity during the classical critical period.

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Visual experience-dependent development of ocular dominance columns in pigmented rats

Cited by 3 publications

References 70 publications

Topographic organization across foveal visual areas in macaques

Topographic organization across foveal visual areas in macaques

Three-dimensional topography of eye-specific domains in the lateral geniculate nucleus of pigmented and albino rats

Development of ocular dominance columns across rodents and other species: revisiting the concept of critical period plasticity

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