Vibrissal afferents from trigeminus to cortices
On each side of the rat’s snout there are five horizontal rows of vibrissae that form an orderly array of low-threshold mechanoreceptors. Each peripheral fiber innervating these mechanoreceptors responds to only one vibrissa and, centrally, the arrangement of the vibrissal pad is mapped into homotopic arrays of cellular aggregates. In layer 4 of the mouse somatosensory cortex in which they were first observed, aggregates consist of small stellate cells surrounding a ‘hollow’ core filled with dendrites, axons and glial cells. Thence the term barrel was used to describe their structure (Woolsey and Van der Loos, 1970). Homotopic cellular aggregates were later observed in the ventral posterior medial nucleus (VPM) of the thalamus and in trigeminal brainstem nuclei (Van der Loos, 1976; Ma and Woolsey, 1984). They were called barreloids and barrelettes respectively. So, to each vibrissa correspond a trigeminal barrelette, a thalamic barreloid, and a cortical barrel. Because of this morphologically demonstrable, homologous arrangement of each of its major component parts, the vibrissal system of rodents has become one of the most valuable models for research in sensory physiology, developmental neuroscience, and in studies of experience-dependent synaptic plasticity. The advent of transgenic mice and the development of new imaging techniques in vivo have further contributed to promote the popularity of this sensory system.
By the mid-nineties we knew of only two pathways of information processing in the vibrissal system of rodents; (1) a lemniscal pathway that arises from the principal trigeminal nucleus (PrV), transits through the VPM, and terminates in layer 4 of the barrel cortex; (2) a paralemniscal pathway whose exact origin was uncertain, that transits through the posterior thalamic nuclear group (Po) and terminates in cortical regions surrounding the barrels. Yet, brainstem neurons that gave rise to these pathways were only partially identified, and it was not clear to what degree vibrissal inputs to the VPM and Po arose from separate populations of trigeminothalamic cells. Since then, tract tracing studies and studies that combined electrophysiological recording with single cell labelling have clarified these issues and led to the discovery of additional pathways. So far, four ascending pathways of vibrissal information have been identified: three pathways that relay information through different sectors of the VPM, and another one through the medial part of Po (Pom). The multiplicity of pathways thus necessitates a revision of the current nomenclature to avoid confusion in the research community. The Text Box below describes the updated nomenclature that will be used in the present review.
| Here we shall refer to the somatosensory thalamic nuclei according to the nomenclature of the Stereotaxic Atlas of the Rat Brain by Paxinos and Watson (1998). Thus, when intranuclear subdivisions do not matter, the ventral posterior medial nucleus and the posterior thalamic nuclear group will be abbreviated as VPM and Po, respectively. However, tract tracing and electrophysiological studies have now identified three pathways that pass through different sectors of the VPM (see Figure 1B). To keep on with names used in prior studies, we shall distinguish two VPM regions: the dorsal medial region (VPMdm) and the ventral lateral region (VPMvl).
We define a pathway as a 3-neuron chain that links the vibrissae to the cerebral cortex: it comprises a trigeminal ganglion cell, a trigeminothalamic neuron, and a thalamocortical cell. There also exist collateral pathways that process vibrissal input through the cerebellum and superior colliculus before sending information to cortex. The organization of the latter pathways is less well documented, and will not be considered in this review. Pathways are to be distinguished from sensory channels, which are subsystems within a pathway that sample different ranges of whisker deflection (rapidly and slowly adapting fibers, low- and high-threshold afferents; Stüttgen et al., 2006). Parallel channels arise from different populations of ganglion cells that are likely associated with different types of nerve endings in whisker follicle.
Vibrissal input in trigeminal nuclei
The brainstem trigeminal complex is the first processing stage in the vibrissal system; it comprises the PrV and the spinal trigeminal nucleus (SpV), which consists of the oralis (SpVo), interpolaris (SpVi) and caudalis (SpVc) subnuclei. The SpVi is further divided into rostral (SpVir) and caudal (SpVic) territories, which correspond to the magno- and parvocellular cytoarchitectonic divisions of Phelan and Falls (1989), respectively (Figure 1). In cytochrome oxidase stained coronal sections of the brainstem, the PrV, SpVic and caudal part of the SpVc display honeycomb-like patches, termed barrelettes, in which primary vibrissa afferents terminate. In each of these subnuclei barrelettes form rostrocaudally-oriented rods, about 1 mm long and 60 µm wide, whose orderly arrangement replicates that of the vibrissae on the mystacial pad (Ma and Woolsey, 1984; Henderson and Jacquin, 1995). Barrelettes are not discernible in the SpVo and SpVir.
Regardless of how they respond to whisker deflection, large caliber vibrissa afferents (Aβ) form ladder-like projection patterns in the brainstem, consisting of several puffs of terminations distributed at regular interval (150-200 µm) in each of the trigeminal nuclei (Hayashi, 1980; Henderson and Jacquin, 1995). The discontinuous arbors from each of the fibers innervating a single whisker interdigitate to produce a rostrocaudally continuous column that is coextensive with the barrelette corresponding to the same vibrissa. Collateral distribution bears no obvious relationship to the functional properties of the axons (Shortland et al., 1996), which indicates that second-order neurons in each subnucleus receive the same sensory messages. Therefore, the parallel pathways that arise from these subnuclei do not relay inputs encoding different features of an object. They likely use the same sensory inputs to inform the brain about whisker motion, texture and shape, and object location in the whisking space (Yu et al., 2006), or again different pathways may operate in different behavioral contexts (e.g., the exploratory and object recognition modes discussed by Curtis and Kleinfeld, 2006).
With regard to the innervation of trigeminal nuclei by vibrissal afferents, the caudalis subnucleus deserves special comment. Like the other subnuclei, the SpVc receives profuse vibrissal input but contains relatively few trigeminothalamic neurons. The bulk of caudalis projections target the other trigeminal nuclei. Therefore, what is conveyed to the thalamus by each of the other subnuclei is already a synthesis of peripheral and caudalis inputs.
Parallel pathways of vibrissal information
Figure 1 shows a wiring diagram that summarizes the anatomical organization of the four ascending pathways of vibrissal information described below.
The lemniscal pathway (1)
The VPM has long been recognized as the thalamic relay station of the lemniscal pathway. It contains a single type of neurons, the relay cells, which are clustered in whisker-related structures called barreloids. Barreloids form curved, obliquely oriented tapering rods that extend from the border of Pom towards the ventral posterior lateral nucleus (Figure 1A; Land et al., 1995; Haidarliu and Ahissar, 2001; Varga et al., 2002). In the ventral lateral part of the VPM (VPMvl), barreloids fade out and become undistinguishable. As described below, that part of the VPM serves as a relay station for a specific population of trigeminothalamic cells. Thus, although the VPMvl does not yet figure in any atlas of the rat’s brain, we shall consider it here as a separate entity (for a topographic description of VPMvl see Haidarliu et al., 2008).
Thalamic barreloids receive vibrissal input principally from small-sized PrV neurons (soma diameter < 20 µm) whose dendrites are confined within the limit of their home barrelette (Henderson and Jacquin, 1995; Lo et al., 1999). These cells have receptive field dominated by a single whisker, and account for about 75% of the projection cells in PrV (Minnery and Simons, 2003). They project only to the contralateral VPMdm, where they give off small bushy terminal fields (~ 80 µm in diameter) in the homologous barreloid. Together, cells within a given PrV barrelette innervate the whole of a barreloid, and their projections show little convergence (on average, a VPMdm relay cell receives input from 1 - 2 PrV neurons; Castro-Alamancos, 2002; Deschênes et al., 2003; Arsenault and Zhang, 2006). Sensory transmission in this fine-grained map of vibrissa representation is mediated by large-sized perisomatic synapses that ensure a fast and secure relay of information (Spacek and Lieberman, 1974; Williams et al., 1994). It is commonly thought that the high spatio-temporal resolution of the lemniscal pathway is ideally suited for texture discrimination.
Like PrV cells, barreloid cells display vigorous, short-latency responses (4 - 6 ms) to deflection of the principal whisker (Minnery et al., 2003). Weaker responses to 1 - 5 surrounding whiskers are also recorded in lightly anesthetized animals, but later responses are eliminated by deepening anesthesia (Friedberg et al., 1999; Aguilar and Castro-Alamancos, 2005), or by lesion of the intersubnuclear projections from the SpV (Timofeeva et al., 2004). Axons of barreloid cells do not branch locally, but give off collaterals in the reticular thalamic nucleus (Rt; Harris, 1987) as they head towards the primary somatosensory cortex (S1), where they innervate profusely layers 3-4 of a barrel column, and more sparsely the upper layer 6 of the same column (Figure 2A; Jensen and Killackey, 1987; Pierret et al., 2000; Arnold et al., 2001). Relay cells in barreloids receive excitatory corticothalamic input from upper lamina 6 cells of a barrel column that is distributed principally over the distal dendrites (Hoogland et al., 1987; Bourassa et al., 1995; Mineff and Weinberg, 2000), and an inhibitory input from Rt cells that targets the whole of the dendritic tree (Peschanski et al., 1983; Ohara and Lieberman, 1993; Varga et al., 2002). At a unitary level, corticothalamic and Rt projections are composed of axons with terminal field topographically restricted to the barreloid representing the principal whisker of their receptive field (Bourassa et al., 1995; Désîlets-Roy et al., 2002). It is worth reminding that the thalamus of rodents (except for the lateral geniculate nucleus) is devoid of local circuit cells; thus, the Rt represents the sole source of inhibitory inputs to all subdivisions of the VPM (Barbaresi et al., 1986).
The lemniscal pathway (2)
At the dorsomedial margin of the VPM, near Pom, there is a stratum of barreloid cells (~ 150 µm thick) that receive vibrissal input from an additional population of PrV cells with large multiwhisker receptive field (Veinante and Deschênes, 1999). Thus, in contrast with VPMc cells whose receptive field is dominated by a single vibrissa, those situated in the head of the barreloids (i.e., in VPMh) respond equally well to multiple vibrissae (Urbain and Deschênes, 2007a). Because of their proximity to Pom, VPMh cells extend dendrites across the VPM/Pom border, which leads to their modulation by corticothalamic fibers from the vibrissa motor cortex that project to Pom.
If VPMc and VPMh relay cells form separate pathways of vibrissal information, one would expect both populations of neurons to differ in the way they innervate the barrel cortex. A recent study indeed demonstrated that VPMh cells project principally to septal regions, whereas VPMc cells innervate mainly the homologous barrel (Furuta et al., 2009). Moreover, septal cells were shown to maintain their multiwhisker receptive field after lesion of the SpV, but that lesion of the PrV abolishes nearly completely vibrissal responses throughout the barrel cortex. These results thus provide conclusive evidence that the multiwhisker receptive field of septal cells derives primarily from their innervation by VPMh cells.
Corticothalamic projections also display specificity with respect to VPMc and VPMh subdivisions. While upper lamina 6 cells of a barrel column establish a one to one reciprocal relationship with the corresponding barreloid, lower lamina 6 cells of a barrel column and lamina 6 cells of septal columns project to Pom, and form rostrocaudally oriented bands in VPMh (Bourassa et al., 1995; Deschênes et al., 1998). Moreover, VPMh cells, but not VPMc cells, receive corticothalamic input from lamina 6 of the vibrissa motor cortex (Urbain and Deschênes, 2007a). A similar topographic specificity characterizes Rt projections to the VPM. Some axons only innervate VPMh, while others give off terminations throughout the whole expanse of a barreloid (Désîlets-Roy et al., 2002). In sum, anatomical and electrophysiological data point to a functional specialization of cells in the head of the barreloids, which suggests that the two subdivisions of the lemniscal pathway that pass through VPMc and VPMh convey different types of vibrissal information.
The extralemniscal pathway
The extralemniscal pathway differs from the lemniscal pathway in that thalamic cells exhibit large multiwhisker receptive fields that are independent of input from the PrV (Bokor et al., 2008). This pathway arises from medium-sized SpVic cells (soma size, 25-30 µm) that respond to multiple whiskers (Veinante et al., 2000a). There is no evidence that these cells innervate other regions of the brainstem or thalamus. In contrast with the small size of the terminal field of PrV axons in a barreloid (diameter ~ 80 µm; Veinante and Deschênes, 1999), individual SpVic axons form larger, rostrocaudally oriented terminal fields in VPMvl (size ~ 100 µm x 250 µm; Veinante et al., 2000a), suggesting a higher degree of input convergence in this nucleus.
The VPMvl is a crescent-shaped region that approximately corresponds to the lower tier of the VPM. It is thicker caudally and thins out rostrolaterally. It was initially identified as a separate relay station after anterograde tracer injection delineated a ventral lateral region in the VPM that receives input from the SpVic (Pierret et al., 2000). There exist no cytoarchitectonic feature or immunohistochemical stain that permits to clearly delineate its boundary with the rest of the VPM (but see Haidarliu et al., 2008). In cytochrome oxidase stained material, VPMvl does not display whisker-like arrangement (i.e., barreloids).
VPMvl relay cells project to the second somatosensory area (S2) and to the dysgranular zone of S1 by means of axon collaterals (Pierret et al., 2000). Projection foci are dense in layers 4 and 6 of S2, and moderate in layers 3, 4, and 6 of S1. VPMvl receives back projections from specific populations of corticothalamic neurons that reside in lamina 6 of S2 and S1, and from a distinct population of multiwhisker Rt cells (Bokor et al., 2008).
Neurons in S2 and in the septal columns of S1 have large receptive fields (Brumberg et al., 1999; Kwegyir-Afful and Keller, 2004). There is no doubt that in anesthetized animals S2 cells derive their response properties directly from the VPMvl, but the actual impact of VPMvl cells on septal neurons remains unknown.
The paralemniscal pathway
The paralemniscal pathway arises from large-sized, multiwhisker cells located in the SpVir (Williams et al., 1994; Veinante et al., 2000a). On their way to the thalamus, SpVir axons send branches into a number of brainstem and diencephalic regions, which include the inferior olive, the pontine nuclei, the perirubral region, the superior colliculus, the anterior pretectal nucleus, and the zona incerta (ZI). In Pom, axons terminate principally in a shell-like region that covers the dorsomedial aspect of VPM, where they make large synaptic contacts with the proximal dendrites of relay neurons (Lavallée et al., 2005).
The labelling of single axons issuing from different parts of Po revealed a heterogeneous population of fibers which, collectively, project across all the somatomotor regions of the neocortex: S1, S2, perirhinal, insular and motor cortices (Deschênes et al., 1998). The great majority of these axons divide in the white matter at their exit from the striatum and send branches in different cortical areas. The laminar distribution of terminal fields varies across areas, but layers 5a and 1 are usually the most densely innervated (Figure 2B). As a rule, cells labelled at the same injection site in Po project to the same cortical regions. Thus, Po appears as a collection of discrete neuronal assemblies that have in common a multiareal projection pattern.
Like most higher-order thalamic nuclei, Po receives a dual corticothalamic input: one that arises from layer 6 cells in cortical areas innervated by Po axons, and another one from layer 5b cells that are exclusively located in the granular and dysgranular zones of the barrel field (Bourassa et al., 1995; Veinante et al., 2000b). Latter projection consists of collaterals of long-range axons that project to the tectum, ZI, and other brainstem regions. These collaterals do not supply a branch in the Rt or in the VPM, but establish large synaptic contacts with the proximal dendrites of Pom neurons (Hoogland et al., 1987, 1991; Bourassa et al., 1995; Groh et al., 2008). These large terminals are morphologically similar to those of trigeminothalamic axons, suggesting a strong excitatory cortical drive.
Inhibitory inputs to Pom arise from three sources: the Rt, the ventral division of ZI (ZIv), and the anterior pretectal nucleus (Barthó et al., 2002; Bokor et al., 2005). While single Rt axons innervate extensive regions of Pom and mostly target distal dendrites (Pinault et al., 1995), incertal and pretectal axons make large GABAergic synaptic contacts on the soma and proximal dendrites, next to the SpVir terminals, which suggests that extrathalamic inhibitory inputs can exert a strong control over sensory transmission in this nucleus. It is not yet known whether incertal and pretectal axons contact different subpopulations of Pom cells.
Control of sensory transmission in Pom
Electrophysiological studies of Pom neurons were probably those that produced the most puzzling results. While anatomical studies reported that Pom received monosynaptic input from the trigeminal nuclei, Pom cells were found to respond weakly to whisker deflection. When present, responses occurred at long latencies 16 - 20 ms), and were of much lower magnitude than those observed in the VPM (Diamond et al., 1992a; Sosnik et al., 2001). Moreover, sensory responses in Pom were suppressed by silencing the barrel cortex, which led to the proposal that sensory transmission in this nucleus depends on cortical feedback (Diamond et al., 1992b). Yet, the reason for which Pom cells responded so weakly and tardily to whisker deflection remained intriguing. This issue was finally resolved after it was shown that Pom receives GABAergic input from the ZIv (Barthó et al., 2002), and that most of the trigeminal axons that innervate Pom also project to the ZIv (Veinante et al., 2000). Thereafter, electrophysiological studies convincingly demonstrated that ZIv cells take part in a feedforward inhibitory circuit that gates vibrissal inputs, and that silencing ZIv reinstates short-latency sensory transmission through Pom (Trageser and Keller, 2004; Lavallée et al., 2005). It was thus proposed that the relay of vibrissal inputs through this nucleus relies on a mechanism of disinhibition (i.e., inhibition of the inhibitory incerto-thalamic pathway). This possibility received support from a recent study in which it was shown that corticofugal messages from the vibrissa motor cortex suppress vibrissal responses in ZIv, and that suppression is mediated by an intra-incertal GABAergic circuit (Figure 3; Urbain and Deschênes, 2007b). Thus, these results suggest that sensory transmission in Pom involves a top-down disinhibitory mechanism that is contingent on motor instructions.
Thalamic projections from the SpVo and SpVc
Thalamic projection from the SpVo arises from large cells with multiwhisker receptive field (Jacquin and Rhoades, 1990; Veinante et al., 2000a). It is the least abundant trigeminothalamic projection, and also the least studied. It terminates in the most posterior part of the VPM and Po, right in front of the pretectum, and also in a caudal thalamic region intercalated between the pretectal and medial geniculate nuclei. These thalamic regions are known to receive multisensory inputs (somatic, visceral, nociceptive, auditory), and to project to the perirhinal cortex, striatum, and amygdala (Groenewegen and Witter, 2004). Oralis cells also provide a substantial projection to the superior colliculus. Although electrophysiological data are not yet available, there is little doubt that the oralis projection constitutes a ‘fifth pathway’ that might be involved in the association of multiple sensory inputs, and the translation of this information via the amygdala and temporal cortices in behavioral and emotional reactions.
The SpVc contains both mono- and multiwhisker responsive cells (Renehan et al., 1986), but so far there exist no clear evidence that these cells project to the thalamus. However the SpVc projects abundantly to the other trigeminal subnuclei (Jacquin et al., 1990a). As far as we know, no physiological study has yet examined vibrissal response properties in this subnucleus.
Anatomical basis for crosstalk between the vibrissal pathways
In the brainstem, the parallel streams of vibrissal information processing are not totally isolated from each other, in that each trigeminal subnucleus that gives rise to an ascending pathway receives projections from the other subnuclei (Figure 4; Jacquin et al., 1990a; Voisin et al., 2002). Although most subnuclei are reciprocally connected, the most abundant intersubnuclear projections are those of the SpVc to the SpVi and PrV, and those from the SpVic to the PrV. The PrV, for instance, receives inhibitory GABAergic projection from the SpVic, and excitatory glutamatergic projection from the SpVc (Furuta et al., 2008). The inhibitory projection is particularly significant since 86% of the SpVic cells that project to the PrV express the transcript for VIAAT, a vesicular inhibitory amino acid transporter that is expressed in both GABAergic and glycinergic neurons. That the SpVic exerts a strong inhibitory control over sensory transmission in the PrV is further supported by the near complete elimination of surround-whisker inhibition in the PrV after lesion of the SpVi (Furuta et al., 2008; see also Lee et al., 2008 for additional evidence obtained in behaving rats).
When retrograde tracers are injected into the SpVi of rodents, the vast majority of retrogradely labeled cells in the brain are found in the other trigeminal nuclei (Jacquin et al., 1990a), in the somatosensory cortical areas (Wise and Jones, 1977; Wise et al., 1979; Killackey et al., 1989), and in cholinergic neurons located in the pedunculo-pontine nucleus (Timofeeva et al., 2005). The projection from S1 is heavy and topographically organized, connecting barrels to homotopic barrelettes in the brainstem (Welker et al., 1988; Jacquin et al., 1990b). The actual impact of these inputs on the activity of intersubnuclear-projecting cells is currently unknown, but available evidence suggest that they can exert a decisive influence on the way trigeminothalamic cells respond to vibrissal inputs (Woolston et al., 1983; Jacquin et al., 1990b; Hallas and Jacquin, 1990; Timofeeva et al., 2005). This raises the possibility that, by controlling the activity of intersubnuclear-projecting cells, brain regions that project to the trigeminal nuclei may take an active part in selecting the type of information that is conveyed through each of the vibrissal pathways.
A central issue in sensory physiology is to understand how an animal endowed with highly sensitive sensory organs, and exploring the environment, can control the unceasing stream of sensory inputs it receives, and select those that are most relevant to an adaptive behavior. Clearly, there should exist multilevel, state-dependent and context-dependent gating mechanisms that filter out irrelevant sensory inputs. For example, when rats whisk to explore a new environment, they are likely little interested in object texture, no more than we are when we stretch out our arms to locate obstacles in a dark room. Processing texture information in this context appears behaviorally irrelevant; therefore pathways that process texture information might be depressed in this condition. Thus, sensory signals associated with different modes of tactual information processing (exploration, object recognition, whisking in air) might be differentially gated in brainstem trigeminal nuclei by inhibitory intersubnuclear projections.
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