Towards a unified scheme of cortical lamination for primary visual cortex across primates: insights from NeuN and VGLUT2 immunoreactivity

Vesicular glutamate transporter (VGLUT) proteins regulate the storage and release of glutamate from synapses of excitatory neurons. Two isoforms, VGLUT1 and VGLUT2, are found in most glutamatergic projections across the mammalian visual system, and appear to differentially identify subsets of excitatory projections between visual structures. To expand current knowledge on the distribution of VGLUT isoforms in highly visual mammals, we examined the mRNA and protein expression patterns of VGLUT1 and VGLUT2 in the lateral geniculate nucleus (LGN), superior colliculus, pulvinar complex, and primary visual cortex (V1) in tree shrews (Tupaia belangeri), which are closely related to primates but classified as a separate order (Scandentia). We found that VGLUT1 was distributed in intrinsic and corticothalamic connections, whereas VGLUT2 was predominantly distributed in subcortical and thalamocortical connections. VGLUT1 and VGLUT2 were coexpressed in the LGN and in the pulvinar complex, as well as in restricted layers of V1, suggesting a greater heterogeneity in the range of efferent glutamatergic projections from these structures. These findings provide further evidence that VGLUT1 and VGLUT2 identify distinct populations of excitatory neurons in visual brain structures across mammals. Observed variations in individual projections may highlight the evolution of these connections through the mammalian lineage.

Section: Primary Visual Cortex (V1)mentioning

confidence: 94%

Distributions of vesicular glutamate transporters 1 and 2 in the visual system of tree shrews (Tupaia belangeri)

Balaram

Isaamullah

Petry

et al. 2015

“…Monoclonal anti‐VGLUT2 (MAB5504, Millipore, Billerica, MA) is a mouse IgG1 antibody with clone 8G9.2, which was developed against the full length of recombinant protein from rat VGLUT2, and labels a single band at 56 kDa (Balaram et al, ). Immunoreactivity of anti‐VGLUT2 accurately recognizes VGLUT2 in primates (Balaram et al, ; Balaram and Kaas, ; Baldwin et al, ; Liao et al, ) and rats (Kaneko and Fujiyama, ).…”

Section: Methodsmentioning

confidence: 99%

Intracortical connections are altered after long‐standing deprivation of dorsal column inputs in the hand region of area 3b in squirrel monkeys

Liao

Reed

Kaas

et al. 2015

Self Cite

A complete unilateral lesion of the dorsal column somatosensory pathway in the upper cervical spinal cord deactivates neurons in the hand region in contralateral somatosensory cortex (areas 3b and 1). Over weeks to months of recovery, parts of the hand region become reactivated by touch on the hand or face. In order to determine if changes in cortical connections potentially contribute to this reactivation, we injected tracers into electrophysiologically identified locations in cortex of area 3b representing the reactivated hand and normally activated face in adult squirrel monkeys. Our results indicated that most of the expected connections of area 3b remained for partially reactivated area 3b, including the majority of intrinsic connections within area 3b; feedback connections from area 1, secondary somatosensory cortex (S2), parietal ventral area (PV) and other cortical areas; and thalamic inputs from the ventroposterior lateral nucleus (VPL). In addition, tracer injections in the reactivated hand region of area 3b labeled more neurons in the face and shoulder regions of area 3b than in normal monkeys, and injections in the face region of area 3b labeled more neurons in the hand region. Unexpectedly, the intrinsic connections within area 3b hand cortex were more widespread after incomplete dorsal column lesions (DCLs) than after a complete DCL. Although these additional connections were limited, these changes in connections may contribute to the reactivation process after injuries.

“…One of the most revealing preparations is to react for the VGluT2 protein which is concentrated in the synaptic terminals of thalamocortical axons (see Balaram et al, ) of the driving type that activates primary cortical areas (Sherman & Guillery, ). Studies in other primates indicate that dense concentrations of VGluT2 protein identify layer 4 and the layer 3 blobs of V1 (e.g., Wong & Kaas, ; Balaram et al, ; Balaram & Kaas, ). Thus, the border of V1–V2 is most apparent in brain sections of flattened cortex in the section containing layer 4 (dark regions in Figure a) or the dark dot like pattern of layer 3 blobs (lower left part of Figure a).…”

Section: Resultsmentioning

confidence: 99%

Architectonic features and relative locations of primary sensory and related areas of neocortex in mouse lemurs

Saraf

Balaram

Pifferi

et al. 2018

Self Cite

Mouse lemurs are the smallest of the living primates, and are members of the understudied radiation of strepsirrhine lemurs of Madagascar. They are thought to closely resemble the ancestral primates that gave rise to present day primates. Here we have used multiple histological and immunochemical methods to identify and characterize sensory areas of neocortex in four brains of adult lemurs obtained from a licensed breeding colony. We describe the laminar features for the primary visual area (V1), the secondary visual area (V2), the middle temporal visual area (MT) and area prostriata, somatosensory areas S1(3b), 3a, and area 1, the primary motor cortex (M1), and the primary auditory cortex (A1). V1 has "blobs" with "nonblob" surrounds, providing further evidence that this type of modular organization might have evolved early in the primate lineage to be retained in all extant primates. The laminar organization of V1 further supports the view that sublayers of layer 3 of primates have been commonly misidentified as sublayers of layer 4. S1 (area 3b) is proportionately wider than the elongated area observed in anthropoid primates, and has disruptions that may distinguish representations of the hand, face, teeth, and tongue. Primary auditory cortex is located in the upper temporal cortex and may include a rostral area, R, in addition to A1. The resulting architectonic maps of cortical areas in mouse lemurs can usefully guide future studies of cortical connectivity and function.