Topographic organization across foveal visual areas in macaques

Hangqi Li; Danling Hu; Hisashi Tanigawa; Toru Takahata

doi:10.3389/fnana.2024.1389067

Topographic organization across foveal visual areas in macaques

Front Neuroanat. 2024 Apr 29:18:1389067. doi: 10.3389/fnana.2024.1389067. eCollection 2024.

Authors

Hangqi Li^{1

2}, Danling Hu^{1

2}, Hisashi Tanigawa^{1

2}, Toru Takahata^{1

2

3}

Affiliations

¹ Key Laboratory for Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, China.
² Interdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University, Hangzhou, China.
³ Department of Neurology of the Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.

Abstract

Introduction: While 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.

Methods: In 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.

Results: V1 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.

Discussion: This study provides valuable insights into the connectivity of the foveal visual cortex, which was ambiguous in previous imaging studies.

Keywords: Macaca mulatta; feedback projection; foveal visual field; retrograde labeling; striate cortex.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was supported by grants from STI 2030-Major Projects (2021ZD0200401) to TT and by National Natural Science Foundation of P. R. China to TT (32170992 and U20A20221) and HT (31872776).