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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.

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.

In primate vision, the encoding of color perception arises from three types of retinal cone cells (L, M, and S cones). The inputs from these cones are linearly integrated into two cone-opponent channels (cardinal axes) before the lateral geniculate nucleus. In subsequent visual cortical stages, color-preferring neurons cluster into functional domains within “blobs” in V1, “thin/color stripes” in V2, and “color bands” in V4. Here, we hypothesize that, with increasing cortical hierarchy, the functional organization of hue representation becomes more balanced and less dependent on cone opponency. To address this question, we used intrinsic signal optical imaging in macaque V1, V2, and V4 cortices to examine the domain-based representation of specific hues (here referred to as “hue domains”) in cone-opponent color space (4 cardinal and 4 intermediate hues). Interestingly, we found that in V1, the relative size of S-cone hue preference domain was significantly smaller than that for other hues. This notable difference was less prominent in V2, and, in V4 was virtually absent, resulting in a more balanced representation of hues. In V2, hue clusters contained sequences of shifting preference, while in V4 the organization of hue clusters was more complex. Pattern classification analysis of these hue maps showed that accuracy of hue classification improved from V1 to V2 to V4. These results suggest that hue representation by domains in the early cortical hierarchy reflects a transformation away from cone-opponency and toward a full-coverage representation of hue.

Because at least some squirrel monkeys lack ocular dominance columns (ODCs) in the striate cortex (V1) that are detectable by cytochrome oxidase (CO) histochemistry, the functional importance of ODCs on stereoscopic 3-D vision has been questioned. However, conventional CO histochemistry or trans-synaptic tracer study has limited capacity to reveal cortical functional architecture, whereas the expression of immediate-early genes (IEGs), c-FOS and ZIF268, is more directly responsive to neuronal activity of cortical neurons to demonstrate ocular dominance (OD)-related domains in V1 following monocular inactivation. Thus, we wondered whether IEG expression would reveal ODCs in the squirrel monkey V1. In this study, we first examined CO histochemistry in V1 of five squirrel monkeys that were subjected to monocular enucleation or tetrodotoxin (TTX) treatment to address whether there is substantial cross-individual variation as reported previously. Then, we examined the IEG expression of the same V1 tissue to address whether OD-related domains are revealed. As a result, staining patterns of CO histochemistry were relatively homogeneous throughout layer 4 of V1. IEG expression was also moderate and homogeneous throughout layer 4 of V1 in all cases. On the other hand, the IEG expression was patchy in accordance with CO blobs outside layer 4, particularly in infragranular layers, although they may not directly represent OD clusters. Squirrel monkeys remain an exceptional species among anthropoid primates with regard to OD organization, and thus are potentially good subjects to study the development and function of ODCs.

Cytochrome oxidase (CO) histochemistry has been used to reveal the cytoarchitecture of the primate brain, including blobs/puffs/patches in the striate cortex (V1), and thick, thin and pale stripes in the middle layer of the secondary visual cortex (V2). It has been suggested that CO activity is coupled with the spiking activity of neurons, implying that neurons in these CO-rich subcompartments are more active than surrounding regions. However, we have discussed possibility that CO histochemistry represents the distribution of thalamo-cortical afferent terminals that generally use vesicular glutamate transporter 2 (VGLUT2) as their main glutamate transporter, and not the activity of cortical neurons. In this study, we systematically compared the labeling patterns observed between CO histochemistry and immunohistochemistry (IHC) for VGLUT2 from the system to microarchitecture levels in the visual cortex of squirrel monkeys. The two staining patterns bore striking similarities at all levels of the visual cortex, including the honeycomb structure of V1 layer 3Bβ (Brodmann's layer 4A), the patchy architecture in the deep layers of V1, the superficial blobs of V1, and the V2 stripes. The microarchitecture was more evident in VGLUT2 IHC, as expected. VGLUT2 protein expression that produced specific IHC labeling is thought to originate from the thalamus since the lateral geniculate nucleus (LGN) and the pulvinar complex both show high expression levels of VGLUT2 mRNA, but cortical neurons do not. These observations support our theory that the subcompartments revealed by CO histochemistry represent the distribution of thalamo-cortical afferent terminals in the primate visual cortex.

Pooja Balaram1, Toru Takahata1, Jon H Kaas1,21Department of Psychology, 2Department of Cell and Molecular Biology, Vanderbilt University, Nashville, TN, USAAbstract: Vesicular glutamate transporters (VGLUTs) control the storage and presynaptic release of glutamate in the central nervous system, and are involved in the majority of glutamatergic transmission in the brain. Two VGLUT isoforms, VGLUT1 and VGLUT2, are known to characterize complementary distributions of glutamatergic neurons in the rodent brain, which suggests that they are each responsible for unique circuits of excitatory transmission. In rodents, VGLUT2 is primarily utilized in thalamocortical circuits, and is strongly expressed in the primary sensory nuclei, including all areas of the visual thalamus. The distribution of VGLUT2 in the visual thalamus and midbrain has yet to be characterized in primate species. Thus, the present study describes the expression of VGLUT2 mRNA and protein across the visual thalamus and superior colliculus of prosimian galagos to provide a better understanding of glutamatergic transmission in the primate brain. VGLUT2 is strongly expressed in all six layers of the dorsal lateral geniculate nucleus, and much less so in the intralaminar zones, which correspond to retinal and superior collicular inputs, respectively. The parvocellular and magnocellular layers expressed VGLUT2 mRNA more densely than the koniocellular layers. A patchy distribution of VGLUT2 positive terminals in the pulvinar complex possibly reflects inputs from the superior colliculus. The upper superficial granular layers of the superior colliculus, with inputs from the retina, most densely expressed VGLUT2 protein, while the lower superficial granular layers, with projections to the pulvinar, most densely expressed VGLUT2 mRNA. The results are consistent with the conclusion that retinal and superior colliculus projections to the thalamus depend highly on the VGLUT2 transporter, as do cortical projections from the magnocellular and parvocellular layers of the lateral geniculate nucleus and neurons of the pulvinar complex.Keywords: lateral geniculate nucleus, superior colliculus, pulvinar, primate, glutamate