The rodent barrel cortex and its main afferent pathways
The rodent barrel cortex has become an attractive preparation to study the neuronal microcircuitry of the neocortical column. Here, the columnar organization of sensory cortices is particularly evident since the barrels in cortical layer 4 can be easily visualized even in living, unstained slices. This allows the characterization of single neocortical neurons and neuronal microcircuits in the framework of a cortical column (Fig. 2); an analysis that is not possible in other sensory cortices such as auditory and visual cortex.
Fig. 2: Anatomical components and hypothetical function of the rodent lemniscal whisker-to-barrel pathway which forms a major part of the trigeminal somatosensory system. A: On the snout, the whisker follicles are indicated by grey circles, except for whisker C1 which is in red (as in all its central representations). Arc 1 whiskers are drawn as black lines touching an object. At each level of the pathway an isomorphic arrangement of neuronal cell groups (Arc 1 in bluish color), reflecting the lay-out of the whiskers on the snout, can be found. These are called barrelettes in the primary trigeminal nucleus of the brainstem, barreloids in the ventrobasal thalamic nucleus and most prominent barrels in the primary somatosensory (barrel) cortex. Included into this scheme is our hypothesis that segregating and integrating cortical circuits (shown as arrows in the cortex) are contained in this pathway which are capable to perform object identification. B: Cytochrome oxidase staining of a tangential section through layer IV of the primary somatosensory cortex shows the regular appearance of intensely stained barrels separated by lightly stained septa. (Fig. by courtesy of Pete Land). C: Acute coronal slice through the barrel cortex of a P19 rat illuminated by Dodt gradient contrast. The barrels in layer IV as such but not their specific whisker identity are clearly identifiable (asterisks) as well as all the cortical layers (Roman numerals) that are in vertical register forming a barrel-related column (modified from Schubert et al., 2007).
The structural and functional organization of the rodent whisker-to-barrel system and various behavioral aspects have been recently described in reviews by members of this Research Unit application (Lübke and Feldmeyer, 2007;Petersen, 2007;Schubert et al., 2007;Brecht, 2007). The rodent primary somatosensory (barrel) cortex shows a high and distinct level of differentiation (Fig. 2) and includes the entire representation of the body (as a “ratunculus” or “musculus”, in analogy to the “homunculus” in human somatosensory cortex) . As illustrated in Fig. 2B, some parts of the body are mapped in a one-to-one fashion (e.g. each whisker to a corresponding barrel in the posteromedial barrel subfield; S1BF (Paxinos and Watson, 1998), whereas other parts are mapped to barrels in a non-one-to-one fashion (e.g. the forepaw digits and palm to the forelimb area barrels; S1FL) and still further body parts are represented in subdivisions of S1 not being modularly organized at all (trunk in S1TR) (Welker and Woolsey, 1974;Chapin and Lin, 1984). On the other hand the neocortical modules (here: barrels), which represent the granular cortex, are embedded in a matrix of dysgranular cortex with different connectional and functional properties (Alloway, 2008). These (inter-barrel) septal regions form a strong functional link with the primary motor cortex. This connectivity also closes the loop from an afferent sensory system to an efferent motor system, a circuit that was recently recognized as a sensory-motor model system (Diamond et al., 2008;Ferezou et al., 2007).
It is now well established that several (3 or more) parallel afferent pathways carry the tactile information from the mechanoreceptors (which are associated with the whisker follicles on the snout) to the barrel cortex (for review see Diamond et al., 2008). The core pathway is the so called lemniscal pathway. Neurons in the principal trigeminal nucleus are clustered into ‘barrelettes’. The axons of these second order neurons cross the midline and travel with the medial lemniscal pathway to the ‘barreloids’ of the ventral posteromedial nucleus of the thalamus (VPMdm; dorsomedial sector). Both barrelettes and barreloids are sets of modules arranged as a topographic map of the whiskers themselves; neurons in a given module respond principally to the somatotopically connected whisker. The axons of VPMdm neurons project to the primary somatosensory cortex (S1), where they terminate in ‘barrels’, dense clusters of mostly spiny stellate neurons in layer IV (Fig. 2).
The other well-established labeled-line projection is the paralemniscal pathway (not shown; (Diamond et al., 1992). Neurons in the rostral part of the interpolar part of the spinal trigeminal nucleus, pars interpolaris are not spatially clustered. They project, among other targets, to the medial portion of the posterior nucleus (POm). The axons of POm neurons project to target neurons (pyramidal cells; Bureau et al., 2006) immediately below the barrels, in layer Va (but also layer I) of S1, S2 and to the primary motor cortex.
The primary central neurons of the extralemniscal pathway are also clustered into whisker-related barrelettes in the caudal part of the spinal trigeminal nucleus, pars interpolaris. They project to the ventrolateral domain of the VPM (VPMvl), where neurons are clustered into the ‘tails’ of the VPMdm barreloids. The axons of VPMvl neurons project to the septa between the barrels of S1 and to the secondary somatosensory cortex (S2) where they probably simultaneously start parallel processing of sensory information in two cortical areas, formerly thought to differ in their hierarchical state.