The barrelettes—architectonic vibrissal representations in the brainstem trigeminal complex of the mouse. Normal structural organization

Abstract

The organization of the brainstem trigeminal complex (BTC) of the mouse is described, with emphasis on the normal organization of the vibrissal representations. Thionin staining for Nissal substance was employed to reveal the cytoarchitecture. Cytochrome oxidase histochemistry was used to reveal the chemoarchitecture. Golgi impregnation methods, in combination with thionin staining, were used to examine the neuronal dendritic morphology within a defined cytoarchitectonic context. An in vitro horseradish peroxidase labelling method was used to study the distribution and morphology of primary trigeminal afferent terminals within the BTC. The BTC consists of four distinct subnuclei: principalis (nVp), oralis (nVo), interpolaris (nVi), and caudalis (nVc). The present study shows that these sub-nuclei can be distinguished from each other on the basis of several anatomical criteria, including the distribution and density of neuronal size classes, histochemical staining intensity, morphology and orientation of neuronal dendrites, and size and texture of primary afferent terminal arbors. Anatomical manifestation of vibrissal representations within the BTC can be described in nVp, nVi, and nVc, but not in nVo. Within the three subnuclei where they are found, anatomical vibrissal representations are composed to architectural subunits that form an overall pattern homeomorphic to the pattern of vibrissae on the face of the animal. Each sub-unit forms a cylindrical tube running in a rostrocaudal orientation within the BTC. These sub-units will be called barrelettes. Cytologically, each barrelette consists of cell-dense "sides," surrounding a practically cell-free "hollow." Individual sub-units are separated by narrow, cell-free "septa." Histochemically, each subunit is manifested as a discrete patch of positive-staining reaction products. Differential interference contrast optics shows that these patches correspond precisely to the barrelette hollows. Evidence is presented to show that the barrelettes are the functional units for the processing of vibrissal sensory information. Terminal arborizations of individual primary afferents seem to be confined to the hollow of single barrelettes. The majority of neurons that form the sides of a barrelette have bitufted dendritic arbors, which project predominantly into the barrelette hollow, although a minority of neurons, particularly in nVi and nVc, also extend part of their dendritic arbors into adjacent barrelette hollows. The barrelette hollows are thus the principal neuropil region in which primary afferents and their target neurons interact. Contacts are made mainly between en passant varicosities and terminal boutons on primary afferent collaterals and dendritic spines and shafts of second order neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Mapping somatosensory connectivity in adult mice using diffusion MRI tractography and super-resolution track density imaging

“…In TDI, the barrelette connectivity map was seen in the coronal view in the ventro-lateral and interpolar regions as shown in cytochrome oxidase staining to demarcate the barrelettes in these regions (Li et al, 1994). Conversely, our results showed that the stereotypical barrelette connectivity map was not clearly detected using TDI in the oral part, consistent with current and previous histologic findings (Belford and Killackey, 1979;Bosman et al, 2011;Ma, 1991;Ma and Woolsey, 1984).…”

“…Our TDI results outline the structural connectivity of the trigeminal nuclei as well as surrounding regions, which were evident using 100 million tracks. Additional 3D features of barrelette structures were observed including the rostro-caudal extent of tracks forming cylinder-shaped tubes (data not shown) (Belford and Killackey, 1979;Ma, 1991). We used cytochrome oxidase staining to detect enzyme activity in trigeminal afferent arbours and their postsynaptic target neurons, revealing the barrelette nuclei (Chiaia et al, 1992).…”

“…The anatomy of the principal trigeminal nucleus, as described by Ma (1991), has a two-kernel peanut shell-shape when viewed in the coronal plane. Anteriorly the waist of the shell forms the hilus, which contains the trigeminus motor nucleus.…”

“…The first sensory relay location of whisker primary afferents are the brainstem barrelettes (Ma, 1991). Second order neurons then project to the ventral posteromedial (VPM) thalamic nucleus via the lemniscal pathway (Bates and Killackey, 1985).…”

Central Projections of Trigeminal Afferents Innervating the Face in Naked Mole‐Rats (Heterocephalus glaber)

“…Recent investigations of the somatosensory cortex of mole-rats and laboratory rats have revealed a series of cytochrome oxidase-dense modules coextensive with the incisor representations at the cortical level (Remple et al, 2003;Henry et al, 2006), and this could be reflected in the brainstem as well. In laboratory rodents, modular representations of sensory surfaces have been found in both neocortex (cortical barrels; Woolsey and Van der Loos, 1970) and the TBNC (Belford and Killackey, 1979;Ma, 1991).…”