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On the existence of mechanoreceptors within the neurovascular unit of the mammalian brain

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Abstract

We describe a set of perivascular interneurons (PINs) with series of fibro-vesicular complexes (FVCs) throughout the gray matter of the adult rabbit and rat brains. PIN–FVCs are ubiquitous throughout the brain vasculature as detected in Golgi-impregnated specimens. Most PINs are small, aspiny cells with short or long (> 1 mm) axons that split and travel along arterial blood vessels. Upon ramification, axons form FVCs around the arising vascular branches; then, paired axons run parallel to the vessel wall until another ramification ensues, and a new FVC is formed. Cytologically, FVCs consist of clusters of perivascular bulbs (PVBs) encircling the precapillary and capillary wall surrounded by end-feet and the extracellular matrix of endothelial cells and pericytes. A PVB contains mitochondria, multivesicular bodies, and granules with a membranous core, similar to Meissner corpuscles and other mechanoreceptors. Some PVBs form asymmetrical, axo-spinous synapses with presumptive adjacent neurons. PINs appear to correspond to the type 1 nNOS-positive neurons whose FVCs co-label with markers of sensory fiber-terminals surrounded by astrocytic end-feet. The PIN is conserved in adult cats and rhesus monkey specimens. The location, ubiquity throughout the vasculature of the mammalian brain, and cytological organization of the PIN–FVCs suggests that it is a sensory receptor intrinsic to the mammalian neurovascular unit that corresponds to an afferent limb of the sensorimotor feed-back mechanism controlling local blood flow.

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Acknowledgements

This work was supported by CONACyT, Grant 1782 to LC and JL-S and by Universidad Nacional Autónoma de México, PAPIIT Grant IG200117 to LC and JL-S. The transgenic hGFAP-GFP mouse line was a generous gift from Dr. Helmut Kettenmann. Authors appreciate the numerous suggestions made from Dr. Carlos Cepeda on our manuscript and thank Gema Martínez-Cabrera, Carlos Lozano-Flores Flores, Lourdes Palma, Elsa Nydia Hernández-Ríos, Martín García, and Rafael Olivares for providing technical assistance. The thorough revision of our manuscript by Jessica González Norris and American Journal Experts is also appreciated.

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  1. Departmento de Neuroiologia del Desarrollo y Fisiología, Instituto de Neurobiología. Campus Juriquilla, Universidad Nacional Autónoma de México, Boulevard Universitario 3001, 76230, Juriquilla, Querétaro, Mexico

    Jorge Larriva-Sahd, Víctor Vargas-Barroso, Alfredo Varela-Echavarría & Luis Concha

  2. Departmento de Neuromorfología Funcional, Instituto Mexicano de Psiquiatría “Ramón de la Fuente Muñiz”, Av. México Xochimilco 101, Delegación Tlalpan, 14370, México DF, Mexico

    Martha León-Olea

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429_2019_1863_MOESM1_ESM.tif

Photomontages showing the structure of the adult rabbit perivascular neuron and its processes along the vascular wall with the Rapid-Golgi. a. Survey picture of a perivascular neuron in the anterior olfactory nucleus. The slender neuronal soma (framed in b) forms a long, unbranched axon (asterisk) and a single dendrite (double asterisk), which divides dichotomously (bottom). b. High-magnification micrograph from the corresponding area framed in a. Note the smooth contour and uniform diameter of the initial axonal segment (asterisk), which contrast with the uneven dendrite (double asterisk) forming sparse spines (sp). c. Distal axon from the corresponding area framed in a. Note the large balloon-like and bulb outgrowths along the axon shaft. d. The axon resolves into a knob and a narrow, terminal process (double arrowhead). Single arrowhead = bulb-like outgrowths. rbc = stacked red blood cells. (TIF 5484 KB)

429_2019_1863_MOESM2_ESM.tif

Photomontages showing the somata and proximal processes of perivascular interneurons (arrows) in the cerebral cortex. a. A row of perivascular interneurons and their processes (arrowheads) in the cat occipital lobe. Notice that the neuronal perikaryon and its processes are embedded in the capillary wall. b. Perivascular interneuron in the monkey parietal cortex. Sections impregnated with the Rapid-Golgi technique. c. Immunohistochemistry to GABA. Survey micrograph illustrating several immuno-positive neurons. d. Immunohistochemistry to NPY. Note the perivascular neuron within the vascular wall. e. Two perivascular neurons immuno-positive to somatostatin. Note that proximal processes encircle the vascular lumen. (TIF 5885 KB)

429_2019_1863_MOESM3_ESM.tif

Camera lucida drawing showing the pattern of ramification of perivascular nerves surrounding a blood vessel piercing the dorsal horn (upper right). An image of the adult rabbit cervical spinal cord is shown. (TIF 9350 KB)

429_2019_1863_MOESM4_ESM.tif

Camera lucida drawings showing twin fibers and fibro-vesicular complexes associated with blood vessels in the brainstem. a. Low medulla oblongata. b. Upper medulla oblongata. c. Pons. A single fibril originating a fibro-vesicular complex along the shaft of a blood vessel in the adult rabbit brain. (TIF 3073 KB)

a

. Survey electron micrograph of the Meissner corpuscle of the adult rat palmar skin. A sensory ending (single asterisk) containing numerous mitochondria and sparse laminated secretory granules (arrow) is encased by the concentric glial lamellae (double asterisks). b. High-magnification image of a sensory ending in a Meissner corpuscle. Note the two secretory granules (arrows) with concentric, laminated cores. c. Enlargement of a perivascular bulb at the same magnification containing a secretory granule (arrow) and a multivesicular body resembling the structures observed in the Meissner corpuscle (b). (TIF 3710 KB)

429_2019_1863_MOESM6_ESM.tif

Sagittal views of the distribution of blood vessels in the adult rat olfactory bulb. Sagittal views. a. A section encompassing the bulbar medulla (M) and cortex (C). Note that ascending blood vessels bound large polygonal areas whose apices anastomose fist and, within the cortex, bound smaller polygonal areas of the neuropil. b. High-magnification image of the bulbar cortex showing the distribution and polygonal arrangement of anastomotic blood vessels. Note the progressively larger caliber of blood vessels upwards. c. Camera lucida drawing showing the convergence of capillary blood vessels from the rostral migratory stream (RMS) to the glomerular layer (GL). Note that blood vessels resolve in venous blood vessels within the glomeruli (shaded) by two routes, namely, by perforating vessels from the bulbar rostral migratory stream (gray arrows) to glomeruli or indirectly, via anastomotic blood vessels. Black arrows = glomerular veins; arrowheads = venous glomerular sinuses. d. Cartoon illustrating a perforating, direct (white) and indirect (black) blood vessel covering from the bulbar medulla (dark gray) and deep cortex (light gray) to the glomerular layer (GL). (TIF 3144 KB)

429_2019_1863_MOESM7_ESM.mp4

High-magnification video of twin fibers forming fibro-vascular complexes. The video initially shows the superficial plane and proceeds throughout a blood vessel outlined in the Online Resource (Fig. 2). Note that axons and tributary fibro-vesicular complexes are embedded in the astrocytic end-feet that appear discontinuous but are homogenously impregnated (light-brown) and surround the blood vessel wall. (MP4 4620 KB)

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Larriva-Sahd, J., León-Olea, M., Vargas-Barroso, V. et al. On the existence of mechanoreceptors within the neurovascular unit of the mammalian brain. Brain Struct Funct 224, 2247–2267 (2019). https://doi.org/10.1007/s00429-019-01863-3

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