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Despite its obvious importance, we still know little about the neuronal circuits that process sensory information, mainly because of the heterogeneity of the various neuronal components that make up these circuits. Recent studies have begun to shed light on the neuronal organisation and circuitry of this complex region. Dorsal horn neurons receive sensory information from primary afferents that innervate the skin and deeper tissues of the body and that respond to specific types of noxious and non- noxious stimuli. These afferents terminate in the dorsal horn with a distribution pattern that is determined by their sensory modality and the region of the body that they innervate. The incoming information is processed by complex circuits involving excitatory and inhibitory interneurons, and transmitted to projection neurons for relay to several brain areas. In addition, nociceptive information is conveyed to the ventral horn and contributes to spinally- mediated nocifensive reflexes. Activity at various points in these circuits can be modulated by axons that descend from the brainstem. The balance between excitation and inhibition is critical for maintaining normal sensory function — blocking inhibitory transmission at spinal levels, for example, can lead to allodynia. Indeed, changes in the function of these circuits have been implicated in the development and maintenance of inflammatory and neuropathic pain. Despite the importance of the dorsal horn in normal sensory processing and in pathological conditions, we still know little about the neuronal circuits that link incoming primary afferents to projection neurons, which constitute its major output. The main reason for this is that the great diversity of dorsal horn neurons has made it difficult to develop a comprehensive classification scheme for either the interneurons or the projection cells. Without such a scheme it is not possible to establish the roles of different neurons within these circuits. In this review I describe the basic neuronal components of the dorsal horn and what we know about the circuits in which they are involved, with particular emphasis on pathways that process nociceptive information. This description will be restricted to laminae I- III of Rexed. Figure 1), as we know more about the organisation of this region than that of the deeper laminae. Moreover, this region includes the major termination zone of nociceptive primary afferents (laminae I and IIo). I also discuss changes that could underlie the abnormal sensations that arise following tissue inflammation and in cases of neuropathic pain. The review is based mainly on findings in the rat, as the majority of the relevant studies have been carried out in this species, but also includes information obtained from other species. For example, many recent studies have been carried out in the mouse, due to the increasing availability of animals in which genes have been knocked out, modified or used to drive expression of green fluorescent protein (GFP). In general, there seems to be a remarkable consistency in neuronal organisation across the species, although there are undoubtedly some differences. Laminar organisation of the dorsal horn and primary afferent inputs. Neuronal components in laminae I- IIIPrimary afferents. Primary afferent axons can be classified by peripheral target (for example, cutaneous, articular or visceral afferents), conduction velocity (which is related to size and myelination), response properties (including sensory modality and the intensity of stimulus necessary to activate them) and neurochemical phenotype (such as peptide expression). These features are interrelated, as most large myelinated cutaneous (A. In general, myelinated low- threshold mechanoreceptive afferents arborise in an area extending from lamina IIi- VI, whereas nociceptive and thermoreceptive A. Recent studies have identified a group of cooling- specific C afferents that terminate in lamina I5, as well as two possible candidates for low- threshold mechanoreceptive C fibres that project to lamina II6,7. Nociceptive C fibres can be divided into two major neurochemical groups: those that contain neuropeptides, such as substance P8, and those that do not. These two groups have distinctive termination zones within the superficial laminae. Non- peptidergic C fibres are mainly associated with the skin, where they innervate the epidermis. Expression of Mas- related G- protein coupled receptor member D (MRGPRD), a sensory neuron- specific G protein- coupled receptor, has recently been shown to define a population of non- peptidergic nociceptive C fibres in the mouse. They have axons that terminate peripherally, in the epidermis, and centrally, in a narrow band within lamina II. The differences in their peripheral and central distributions suggest that peptidergic and non- peptidergic nociceptive C fibres differ in function. This view is supported by a recent study in which ablation of the MRGPRD afferents in adult mice resulted in a selective loss of sensitivity to noxious mechanical (but not thermal) stimuli. Determining the relative proportions of primary afferents that belong to each of these classes is difficult. Most of the anatomical studies involving cell counts in dorsal root ganglia have not been corrected for the sampling bias that results from variation in cell sizes, and electrophysiological recordings from nerves are inevitably biased towards larger axons. However, it has been estimated that in the rat around 8. C fibres are peptidergic. All primary afferents use glutamate as their major fast transmitter, and thus have an excitatory action on their postsynaptic targets. However, their ultrastructural appearance and synaptic arrangements differ. Those belonging to non- peptidergic C fibres and A. Central terminals of A. By contrast, peptidergic primary afferents receive few axoaxonic synapses. Descending inputs. Two descending monoamine- containing pathways project to the dorsal horn: a serotonergic system originating mainly in the nucleus raphe magnus, and a noradrenergic pathway from the locus coeruleus and other pontine regions. Both serotonergic and noradrenergic axons terminate diffusely throughout the dorsal horn, and although some form synapses, much of their action is mediated through volume transmission. Another descending pathway that is likely to have a role in pain mechanisms consists of GABA (. They include virtually all of the neurons in lamina II, and most of those in laminae I and III. Interneurons can be divided into two main classes: excitatory (glutamatergic) and inhibitory. The inhibitory interneurons use GABA and/or glycine as their main neurotransmitter(s), and their cell bodies can be identified with antibodies against these amino acids. In the rat, GABA is present in ~2. I, II and III, respectively. Glycine is present at high levels in many lamina III neurons and some of those in laminae I- II, but within laminae I- III glycine immunostaining is largely restricted to GABA- containing cells. This suggests that many inhibitory interneurons co- release GABA and glycine, whereas the others only release GABA. However, electrophysiological studies have identified synapses in this region that are purely glycinergic. Although these may involve axons that originate from glycinergic neurons located outside laminae I- III, in many cases the lack of a GABAergic component probably results from the absence of GABAA receptors at these synapses. The axons of inhibitory interneurons can be identified with antibodies against the vesicular GABA transporter (VGAT, which also transports glycine), glutamate decarboxylase (GAD, the GABA- synthesizing enzyme), or the neuronal glycine transporter (Gly. T2). These reveal a dense plexus of inhibitory axons in laminae I- III, most of which originate from local interneurons. There are no reliable immunocytochemical markers for the cell bodies of glutamatergic neurons, but it is likely that all dorsal horn neurons that are not immunoreactive for GABA or glycine are glutamatergic. Their axons can be identified by the presence of vesicular glutamate transporters (VGLUTs)2. VGLUT2. 28- 3. 0. There are numerous VGLUT2- containing boutons in laminae I- III, most of which originate from local excitatory interneurons. Although there have been several attempts to classify interneurons in laminae I- III, we still do not have a generally accepted scheme that covers all of these cells. Many studies have investigated morphology in the hope of defining specific classes, initially using the Golgi technique, and more recently, with single- cell labelling during electrophysiological recordings. Electrophysiological criteria for determining interneuron subtypes include synaptic inputs from different classes of primary afferent and firing patterns in response to injected current. Several patterns have been described, and among these the delayed, gap and reluctant firing patterns are thought to result from an A- type potassium current (IA)3. Kv. 4. 2 or Kv. 4. Lamina II interneurons have been studied extensively, and the most widely accepted classification scheme for these cells is that developed by Perl and colleagues. They identified four main classes: islet, central, vertical and radial cells, which differed in dendritic morphology (Figure 2). Two recent electrophysiological studies in slices of rat spinal cord used immunocytochemistry to identify the neurotransmitter phenotype of lamina II interneurons, allowing a direct comparison of morphology and function. |
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