Abstract
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.
Highlights
The primate visual system is subdivided into multiple parallel pathways, and this segregation appears as laminar and columnar domains in the visual cortex (Sincich and Horton, 2005)
Correspondence Between Cytochrome oxidase (CO) and vesicular glutamate transporter 2 (VGLUT2)-ir metabolic enzyme found in mitochondria, and its enzymatic activity is coupled with neuronal activity, which is indicated by decreased CO expression in ocular dominance columns (ODCs) that occurs after monocular inactivation (Horton and Hedley-Whyte, 1984; Wong-Riley, 1989)
72.5 ± 1.8% of CO blob area was coincided with VGLUT2-ir patches, and 64.8 ± 0.1% of VGLUT2-ir patch area was coincided with CO blob area, indicating that a majority of each area overlaps with each other
Summary
The primate visual system is subdivided into multiple parallel pathways, and this segregation appears as laminar and columnar domains in the visual cortex (Sincich and Horton, 2005) Some of these domains have been revealed using cytochrome oxidase (CO) histochemistry, such as blobs/puffs/patches in superficial layers of V1 as well as thick, thin, and pale stripes in the middle layer of V2 (Horton and Hubel, 1981; Horton and Hocking, 1996). Previous researchers thought that neurons in CO-rich domains are more active than those outside the domains We questioned this paradigm (Takahata, 2016), since neurons in the V1 blobs and V2 stripes do not show higher expression of immediate-early genes (IEGs), which is more directly coupled with neuronal spiking activity (Kim et al, 2010), compared to neurons outside V1 blobs or V2 dark stripes. We consider that the thalamo-cortical afferent terminals may possess higher metabolic activity than the soma or axons of cortical neurons in general, and CO histochemistry reflects the distribution of thalamo-cortical axons and afferent terminals, rather than the spiking activity of cortical neurons when the cortex is stained (Takahata, 2016)
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