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Neuroscience Letters 367 (2004) 394–398 Thalamocortical projection from the ventral posteromedial nucleus sends its collaterals to layer I of the primary somatosensory cortex in rat Satoko Odaa,∗ , Kiyoshi Kishia , Junli Yanga , Shaoyun Chena , Junko Yokofujitaa , Hiroaki Igarashia , Sachiko Tanihatab , Masaru Kurodaa a Department of Anatomy, Toho University School of Medicine, 5-21-16 Ohmorinishi, Ohta-ku, Tokyo 143-8540, Japan b Department of Pharmacology, Toho University School of Medicine, Ohta-ku, Tokyo 143-8540, Japan Received 24 April 2004; received in revised form 9 June 2004; accepted 16 June 2004 Abstract Here we examined quantitatively axonal projections originating from the ventral posteromedial thalamic nucleus (VPM) to layer I of the primary somatosensory cortex (SI) by extracellular and intracellular injections of biocytin as an anterograde tracer. Following the extracellular injections, two types of VPM afferents with different arborization patterns in SI were observed. The type I extended vertically, forming dense plexus in layers IV and VI, and projected collaterals to layer I. The type II rarely branched in SI, converged in the plexus formed by the type I, and projected no collaterals to the supragranular layers. The labeled fibers in layer I derived from the first type ran parallel to the brain surface, and their mean length was 339.7 ± 87.5 m. Intracellular injection into VPM neurons bearing both types of afferent demonstrated the full axonal arborization in both the reticular thalamic nucleus (Rt) and SI. The total length of the axon of a neuron bearing the type I was 86,968.8 m, and the length of axonal collaterals in layer I of SI was 433.1 m. The total axonal length of a neuron bearing the type II was very small. The present study is the first to demonstrate substantial projections from VPM to layer I of SI, and provide quantitative data on the entire extent of the axonal arborization of thalamocortical projections from single VPM neurons. © 2004 Elsevier Ireland Ltd. All rights reserved. Keywords: Somatosensory system; Thalamocortical pathway; VPM; Rat The thalamocortical pathways, which relay trigeminal somatosensory information from subcortical structures to the primary somatosensory cortex (SI), consist of a specific pathway originating from the ventral posteromedial thalamic nucleus (VPM) and a nonspecific pathway from the posterior nucleus (Po) [9]. Afferent fibers from VPM form dense plexus in both layers IV and VI in cortical columns in SI, whereas those from Po distribute to all layers in the septa between cortical columns and layer I in cortical columns. Thus, it has been considered that these projections are complementary to each other [14,19]. Using extracellular injections of an anterograde tracer, Lu and Lin [13] first demonstrated that VPM ∗ Corresponding author. Tel.: +81 3 5493 5411x2323; fax: +81 3 5493 5437. E-mail address: [email protected] (S. Oda). 0304-3940/$ – see front matter © 2004 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2004.06.042 also projects to layer I of SI. This study, however, could not rule out the possibility that the tracer was absorbed by Po axons in VPM, where Po thalamocortical axons pass mediolaterally. Cauller et al. [4] also found retrogradely labeled VPM neurons after a retrograde tracer application in layer I of the SI. Previous studies using single-fiber labeling methods, however, have shown no substantial projections to layer I [2,3,11,18,21]. Recent studies have shown that specific thalamocortical pathways from the medial geniculate nucleus in the auditory system and the ventral lateral nucleus in the motor system send their fibers to layer I of the primary auditory cortex and the frontal/premotor cortices, respectively [6,15]. Because layer I of SI receives many afferents from various regions, it seems that it is an important site for cortical information processing [4]. The purpose of the present study was to examine quantitatively specific thalamocortical projections of the S. Oda et al. / Neuroscience Letters 367 (2004) 394–398 somatosensory system from VPM to SI, particularly layer I, using extracellular and intracellular labeling methods. Ten male Sprague–Dawley rats (400–620 g) were used in this study. Two of these animals were used for extracellular injection experiments, and the others were for intracellular injection experiments. All injections were administered bilaterally. All animal treatments and care were in accordance with the European Communities Council Directive of 24 November 1986. The animals were anesthetized with 20% urethane or 5.6% chloral hydrate (i.p.) and placed in a stereotaxic apparatus. Cerebrospinal fluid was drained from the cisterna magna to maintain brain stability. The stereotaxic coordinates were obtained from the brain atlas of Paxinos and Watson [17]. For intracellular injections, recording glass micropipettes filled with 2.5% biocytin in 0.05 M Tris buffer (pH 7.3) containing 0.5 M KCl were inserted into VPM with a low-depolarizingcurrent pulse (0.1 nA: 500 ms duration at 1 Hz) to detect silent cells [20]. After the cells were impaled, biocytin was injected 395 by passing 2 or 3 nA depolarizing-current pulses (500 ms duration at 1 Hz) for 10–30 min. Extracellular injections were administered using glass micropipettes (10–15 m in tip diameter) for 10–15 min at a positive current of 5 A in a cycle of 7 s on and 7 s off. The survival times were 6–8 h for intracellular injections and 45–48 h for extracellular injections. The methods for the preparation of 80 m thick serial sections and the visualization of the tracer were according to Chen et al. [7]. The sections were mounted on slides and then counterstained with thionin. The images of biocytin-labeled somata, dendrites, and axons observed under a microscope (Olympus) equipped with a drawing tube were traced. They were reconstructed in coronal plane serial sections viewed with the aid of a 40× objective. For quantitative analysis, axonal segment length was measured using a pen-type map meter and estimated from the measured length and 80 m section thickness. Fig. 1A shows an example of extracellular injection into VPM. Two cortical columns in SI were labeled by this Fig. 1. Example of extracellular injection into VPM. (A) Photomicrograph of site of injection into VPM. (B) Photomicrograph of a labeled fiber plexus in SI. This plexus is mainly formed by vertically extending fibers (indicated by arrows). Two transversally running fibers (indicated by arrowheads) toward the plexus is also observed. (C) Photomicrograph of labeled fiber in layer I of SI. (D) Drawing of reconstructed fibers in layer I (1–5) and superficial region of layer II (6, 7). eml, external medullary lamina; Rt, reticular thalamic nucleus; VPL, ventral posterolateral thalamic nucleus; VPM, ventral posteromedial thalamic nucleus. Scale bars, 1 mm (A), 0.1 mm (B and C), and 0.2 mm (D). 396 S. Oda et al. / Neuroscience Letters 367 (2004) 394–398 Fig. 2. Example of intracellular injection into VPM. (A) Photomicrograph of labeled VPM neurons, A-cell and B-cell. (B) Drawing of axonal trunks from A-cell and B-cell. They branched into collaterals in Rt (a1 and b1) and SI (a2 and b2). Drawings of each axonal arborization in Rt (C) and SI (D). CPu, caudate putamen; ic, internal capsule; LGP, lateral globus pallidus; Rt, reticular thalamic nucleus; VPM, ventral posteromedial thalamic nucleus; and WM, white matter. Scale bars, 0.1 mm (A), 1 mm (B), and 0.2 mm (C and D). S. Oda et al. / Neuroscience Letters 367 (2004) 394–398 injection. In these columns, labeled axonal fibers formed dense plexus in layers IV and VI. Most of these fibers extended vertically in the columns and were highly branched (indicated by arrows in Fig. 1B). Different types of axon were also present. They entered SI distant from target sites, extended toward the brain surface, then sharply turned toward the plexus in layers IV and VI, and converged in the plexus (indicated by arrowheads in Fig. 1B). The axons had few branches and did not project to the supragranular layers. In two of four extracellular injections, a few labeled fibers were observed in layer I (Fig. 1C). Labeled fibers in layer I and the adjacent region in a labeled column were reconstructed (Fig. 1D). The mean length ± S.D. of labeled fibers in layer I was 339.7 ± 87.5 m (n = 6 from two injections; range, 218.3–432.8 m). Some of these fibers originated from the plexus in layer IV of the underlying column. We injected 12 neurons intracellulary; however, both the neuronal dendrites and distal ends of cortical collaterals could be traced completely in two neurons. Fig. 2A shows a pair of intracellulary labeled VPM neurons with overlapping dendritic fields, hereafter called “A-cell” and “B-cell”. They were located in the dorsomedial part of VPM. The A-cell soma was ovoid and its long and short axes were 26.6 and 12.5 m, respectively. This neuron had thick dendrites, and the total dendritic length was 9494.1 m. The B-cell soma was similar to A-cell soma in shape and its long and short axes were 23.4 and 10.9 m, respectively. It had rather slender dendrites and the total dendritic length was 7086.7 m. The morphological features of both neurons agreed with the report of Ohara and Havton [16] in which the dendritic architecture of rat somatosensory thalamic neurons was detailed. Both axonal trunk pathways are shown in Fig. 2B. Their axonal collaterals branched only in the reticular thalamic nucleus (Rt) and SI (Fig. 2C and D). The arborization patterns of collaterals from each axonal trunk in Rt differed. A-cell axonal collaterals (a1) were highly branched and extended long distances, whereas B-cell axonal collaterals (b1) were short and less branched. Their terminal fields in Rt did not overlap. The arborization patterns of collaterals from each axonal trunk in SI illustrated in Fig. 2D also differed. A-cell axonal collaterals (a2) were thick and highly branched, and extended to a cortical column. They formed dense plexus in layer IV and in the superficial part of layer VI. Some axonal branches from the plexus extended to the supragranular layers including layer I. B-cell axonal collaterals (b2) were rarely branched and transversely converged in the plexus of A-cell fiber arborization. They did not project to the supragranular layers. The estimated axonal lengths of A-cell, a standard type of VPM neuron, were examined. The total axonal length was 86,968.8 m, and the lengths of axonal collaterals in Rt and the different layers of SI were 3548.4 m (Rt), 433.1 m (I), 8600.6 m (II/III), 45,096.8 m (IV), 10,862.6 m (V), and 14,757.3 m (VI). The ratios of fiber length of the layers were 0.5 (I), 10.8 (II/III), 56.5 (IV), 13.6 (V), and 18.5% (VI). The estimated lengths of B-cell axonal collaterals were also examined. Its total axonal length was 10,933.9 m, and 397 the lengths of axonal collaterals in Rt and the different layers of SI were 297.8 m (Rt), 0 m (I–III), 783.1 m (IV), 1276.2 m (V), and 3533.5 m (VI). The present study using extracellular and intracellular labeling methods is the first to demonstrate the few but substantial projections to layer I of SI from VPM. Lu and Lin [13] reported that VPM fibers in layer I are short and run vertically to the brain surface, whereas Po fibers run transversely. The present study shows that most of the VPM fibers in layer I are longer, and run parallel to the brain surface. Layer I of SI receives various afferents from the secondary somatosensory cortex (SII), agranular insular cortex, homotopic area of contralateral SI, and Po. These excitatory afferents have been considered as effective elements that act on the pyramidal neurons of layers II/III. Thus, layer I seems to be one of the synaptic convergence sites of the somatosensory system [4,5]. VPM afferent fibers in layer I were short and seemed to be restricted to the width of the underlying cortical columns. On the other hand, Po afferents, which are also thalamic afferents, were long and extended horizontally across the underlying columns. Thus, these two types of thalamocortical afferent seem to participate in the synaptic convergence in layer I in a different manner. The present study also showed that the proportion of VPM fibers in layer I of SI is much smaller than that in other thalamocortical systems, such as in the auditory system [6,8]. This finding supports the physiological evidence that somatosensory information received in layer IV is transmitted to the supragranular layers polysynaptically within a column [1]. Second, two types of VPM afferent with different arborization patterns in SI were observed in both experiments. The first type was the standard type of VPM afferent, which extended vertically forming dense plexus in layers IV and VI, and projected collaterals to layer I. The second type was rarely branched in both Rt and SI, transversely converged in the fiber plexus formed by the first type of afferent, and projected no collaterals to the supragranular layers. Lorente de Nó classified somatosensory cortical afferent fibers that apparently to originate from the thalamus into three types. The second type of fibers in this study seems to be included in the third type (k in Fig. 25) of his classification on the basis of its branching patterns [12]. However, our second type sends no collaterals to the supragranular layers, whereas his third type sends fibers to layer III. Because about 40% of VPM axons in Rt have short, simple branches, the second type of afferent to SI may constitute a significant proportion of VPM thalamocortical projections [10]. At present, it is not known whether or not VPM neurons bearing different types of afferent have distinct physiological properties. 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