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Erschienen in: Surgical and Radiologic Anatomy 9/2011

01.11.2011 | Original Article

The morphological characteristics of corticostriatal and thalamostriatal neurons and their intrastriatal terminals in rats

verfasst von: Bingbing Liu, Lisi Ouyang, Shuhua Mu, Yaxi Zhu, Keyi Li, Mali Zhan, Zongwei Liu, Yu Jia, Wanlong Lei

Erschienen in: Surgical and Radiologic Anatomy | Ausgabe 9/2011

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Abstract

Purpose

The glutamatergic projection from the cerebral cortex and the thalamus extensively innervates the neostriatal neurons. However, some conflicts in the published literatures about cortical and thalamic intrastriatal synaptic terminals still need to be resolved. The present study intends to further elucidate the morphological characteristics of these two types of the terminals and their neurons.

Methods

The corticostriatal and thalamostriatal terminals were immunolabeled for vesicular glutamate transporter type 1 (VGluT1) and 2 (VGluT2), respectively, and their neurons were retrograde labeled by biotinylated dextran amine 3,000 molecular weight (BDA3k) injection into the dorsolateral striatum of rats. The characteristics of the corticostriatal and thalamostriatal terminals were observed at the LM and EM levels, and the data were statistically analyzed with SPSS10.0 software.

Results

We observed that 63.53% of VGluT1+ terminals synapsed on dendritic spines, which was different from VGluT2+ terminals with the equal percentage of synapses on spines and dendrites (14.88 and 17.86%, respectively). Notably, VGluT1+ axospinous synaptic terminals were remarkably larger than VGluT2+ axospinous synaptic terminals. Terminal size-frequency distribution analysis showed that VGluT1+ terminals were within the size ranges of 0.4–0.5 and 0.8–0.9 μm, and VGluT2+ terminals were in the ranges of 0.4–0.5 and 0.6–0.7 μm. Perforated-postsynaptic densities (-PSDs) were more frequently found in VGluT1+ axospinous synaptic terminals than in VGluT2+ axospinous terminals. Furthermore, BDA3k-labeled corticostrital neurons were larger in perikaryal diameter than the thalamostriatal neurons, and they were also categorized as the two main populations based on their size-frequency distribution.

Conclusions

The morphological characteristics of corticostriatal and thalamostriatal terminals and neurons have implications for understanding the roles of synaptic plasticity in adaptive motor control by the basal ganglia, and they have facilitations for understanding the complexities of basal ganglia function.
Literatur
1.
Zurück zum Zitat Albin RL, Gilman S (1989) Parasagittal zonation of GABA-B receptors in molecular layer of rat cerebellum. Eur J Pharmacol 173(1):113–114PubMedCrossRef Albin RL, Gilman S (1989) Parasagittal zonation of GABA-B receptors in molecular layer of rat cerebellum. Eur J Pharmacol 173(1):113–114PubMedCrossRef
2.
Zurück zum Zitat Calabresi P, Centonze D, Gubellini P, Marfia GA, Pisani A, Sancesario G, Bernardi G (2000) Synaptic transmission in the striatum: from plasticity to neurodegeneration. Prog Neurobiol 61(3):231–265PubMedCrossRef Calabresi P, Centonze D, Gubellini P, Marfia GA, Pisani A, Sancesario G, Bernardi G (2000) Synaptic transmission in the striatum: from plasticity to neurodegeneration. Prog Neurobiol 61(3):231–265PubMedCrossRef
3.
Zurück zum Zitat Dhanrajan TM, Lynch MA, Kelly A, Popov VI, Rusakov DA, Stewart MG (2004) Expression of long-term potentiation in aged rats involves perforated synapses but dendritic spine branching results from high-frequency stimulation alone. Hippocampus 14(2):255–264. doi:10.1002/hipo.10172 PubMedCrossRef Dhanrajan TM, Lynch MA, Kelly A, Popov VI, Rusakov DA, Stewart MG (2004) Expression of long-term potentiation in aged rats involves perforated synapses but dendritic spine branching results from high-frequency stimulation alone. Hippocampus 14(2):255–264. doi:10.​1002/​hipo.​10172 PubMedCrossRef
5.
Zurück zum Zitat Dube L, Smith AD, Bolam JP (1988) Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol 267(4):455–471. doi:10.1002/cne.902670402 PubMedCrossRef Dube L, Smith AD, Bolam JP (1988) Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol 267(4):455–471. doi:10.​1002/​cne.​902670402 PubMedCrossRef
7.
Zurück zum Zitat Gerfen CR (1992) The neostriatal mosaic: multiple levels of compartmental organization. J Neural Transm Suppl 36:43–59PubMed Gerfen CR (1992) The neostriatal mosaic: multiple levels of compartmental organization. J Neural Transm Suppl 36:43–59PubMed
9.
Zurück zum Zitat Green A, Peters TJ, Webster DJ (1991) An assessment of academic performance and personality. Med Educ 25(4):343–348PubMedCrossRef Green A, Peters TJ, Webster DJ (1991) An assessment of academic performance and personality. Med Educ 25(4):343–348PubMedCrossRef
10.
Zurück zum Zitat Haber S, McFarland NR (2001) The place of the thalamus in frontal cortical-basal ganglia circuits. Neuroscientist 7(4):315–324PubMedCrossRef Haber S, McFarland NR (2001) The place of the thalamus in frontal cortical-basal ganglia circuits. Neuroscientist 7(4):315–324PubMedCrossRef
11.
Zurück zum Zitat Hisano S, Hoshi K, Ikeda Y, Maruyama D, Kanemoto M, Ichijo H, Kojima I, Takeda J, Nogami H (2000) Regional expression of a gene encoding a neuron-specific Na(+)-dependent inorganic phosphate cotransporter (DNPI) in the rat forebrain. Brain Res Mol Brain Res 83(1–2):34–43PubMedCrossRef Hisano S, Hoshi K, Ikeda Y, Maruyama D, Kanemoto M, Ichijo H, Kojima I, Takeda J, Nogami H (2000) Regional expression of a gene encoding a neuron-specific Na(+)-dependent inorganic phosphate cotransporter (DNPI) in the rat forebrain. Brain Res Mol Brain Res 83(1–2):34–43PubMedCrossRef
12.
Zurück zum Zitat Ichinohe N, Iwatsuki H, Shoumura K (2001) Intrastriatal targets of projection fibers from the central lateral nucleus of the rat thalamus. Neurosci Lett 302(2–3):105–108PubMedCrossRef Ichinohe N, Iwatsuki H, Shoumura K (2001) Intrastriatal targets of projection fibers from the central lateral nucleus of the rat thalamus. Neurosci Lett 302(2–3):105–108PubMedCrossRef
13.
Zurück zum Zitat Johnston JG, Gerfen CR, Haber SN, van der Kooy D (1990) Mechanisms of striatal pattern formation: conservation of mammalian compartmentalization. Brain Res Dev Brain Res 57(1):93–102PubMedCrossRef Johnston JG, Gerfen CR, Haber SN, van der Kooy D (1990) Mechanisms of striatal pattern formation: conservation of mammalian compartmentalization. Brain Res Dev Brain Res 57(1):93–102PubMedCrossRef
15.
Zurück zum Zitat Koshimizu Y, Wu SX, Unzai T, Hioki H, Sonomura T, Nakamura KC, Fujiyama F, Kaneko T (2008) Paucity of enkephalin production in neostriatal striosomal neurons: analysis with preproenkephalin-green fluorescent protein transgenic mice. Eur J Neurosci 28(10):2053–2064. doi:10.1111/j.1460-9568.2008.06502.x PubMedCrossRef Koshimizu Y, Wu SX, Unzai T, Hioki H, Sonomura T, Nakamura KC, Fujiyama F, Kaneko T (2008) Paucity of enkephalin production in neostriatal striosomal neurons: analysis with preproenkephalin-green fluorescent protein transgenic mice. Eur J Neurosci 28(10):2053–2064. doi:10.​1111/​j.​1460-9568.​2008.​06502.​x PubMedCrossRef
16.
Zurück zum Zitat Lapper SR, Bolam JP (1992) Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat. Neuroscience 51(3):533–545PubMedCrossRef Lapper SR, Bolam JP (1992) Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat. Neuroscience 51(3):533–545PubMedCrossRef
17.
Zurück zum Zitat Lei W, Jiao Y, Del Mar N, Reiner A (2004) Evidence for differential cortical input to direct pathway versus indirect pathway striatal projection neurons in rats. J Neurosci 24(38):8289–8299PubMedCrossRef Lei W, Jiao Y, Del Mar N, Reiner A (2004) Evidence for differential cortical input to direct pathway versus indirect pathway striatal projection neurons in rats. J Neurosci 24(38):8289–8299PubMedCrossRef
18.
Zurück zum Zitat Matsumoto N, Minamimoto T, Graybiel AM, Kimura M (2001) Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J Neurophysiol 85(2):960–976PubMed Matsumoto N, Minamimoto T, Graybiel AM, Kimura M (2001) Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J Neurophysiol 85(2):960–976PubMed
20.
Zurück zum Zitat McGuire PK, Bates JF, Goldman-Rakic PS (1991) Interhemispheric integration: II. Symmetry and convergence of the corticostriatal projections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) of the rhesus monkey. Cereb Cortex 1(5):408–417PubMedCrossRef McGuire PK, Bates JF, Goldman-Rakic PS (1991) Interhemispheric integration: II. Symmetry and convergence of the corticostriatal projections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) of the rhesus monkey. Cereb Cortex 1(5):408–417PubMedCrossRef
21.
Zurück zum Zitat Nicholson DA, Yoshida R, Berry RW, Gallagher M, Geinisman Y (2004) Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J Neurosci 24(35):7648–7653PubMedCrossRef Nicholson DA, Yoshida R, Berry RW, Gallagher M, Geinisman Y (2004) Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J Neurosci 24(35):7648–7653PubMedCrossRef
23.
Zurück zum Zitat Raju DV, Shah DJ, Wright TM, Hall RA, Smith Y (2006) Differential synaptology of vGluT2-containing thalamostriatal afferents between the patch and matrix compartments in rats. J Comp Neurol 499(2):231–243. doi:10.1002/cne.21099 PubMedCrossRef Raju DV, Shah DJ, Wright TM, Hall RA, Smith Y (2006) Differential synaptology of vGluT2-containing thalamostriatal afferents between the patch and matrix compartments in rats. J Comp Neurol 499(2):231–243. doi:10.​1002/​cne.​21099 PubMedCrossRef
24.
Zurück zum Zitat Reiner A, Anderson KD (1990) The patterns of neurotransmitter and neuropeptide co-occurrence among striatal projection neurons: conclusions based on recent findings. Brain Res Brain Res Rev 15(3):251–265PubMedCrossRef Reiner A, Anderson KD (1990) The patterns of neurotransmitter and neuropeptide co-occurrence among striatal projection neurons: conclusions based on recent findings. Brain Res Brain Res Rev 15(3):251–265PubMedCrossRef
25.
Zurück zum Zitat Reiner A, Jiao Y, Del Mar N, Laverghetta AV, Lei WL (2003) Differential morphology of pyramidal tract-type and intratelencephalically projecting-type corticostriatal neurons and their intrastriatal terminals in rats. J Comp Neurol 457(4):420–440. doi:10.1002/cne.10541 PubMedCrossRef Reiner A, Jiao Y, Del Mar N, Laverghetta AV, Lei WL (2003) Differential morphology of pyramidal tract-type and intratelencephalically projecting-type corticostriatal neurons and their intrastriatal terminals in rats. J Comp Neurol 457(4):420–440. doi:10.​1002/​cne.​10541 PubMedCrossRef
26.
Zurück zum Zitat Smith Y, Raju DV, Pare JF, Sidibe M (2004) The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci 27(9):520–527PubMedCrossRef Smith Y, Raju DV, Pare JF, Sidibe M (2004) The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci 27(9):520–527PubMedCrossRef
27.
Zurück zum Zitat Tsvetkov E, Carlezon WA, Benes FM, Kandel ER, Bolshakov VY (2002) Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 34(2):289–300PubMedCrossRef Tsvetkov E, Carlezon WA, Benes FM, Kandel ER, Bolshakov VY (2002) Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 34(2):289–300PubMedCrossRef
28.
Zurück zum Zitat Van der Werf YD, Witter MP, Groenewegen HJ (2002) The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Brain Res Rev 39(2–3):107–140PubMedCrossRef Van der Werf YD, Witter MP, Groenewegen HJ (2002) The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Brain Res Rev 39(2–3):107–140PubMedCrossRef
Metadaten
Titel
The morphological characteristics of corticostriatal and thalamostriatal neurons and their intrastriatal terminals in rats
verfasst von
Bingbing Liu
Lisi Ouyang
Shuhua Mu
Yaxi Zhu
Keyi Li
Mali Zhan
Zongwei Liu
Yu Jia
Wanlong Lei
Publikationsdatum
01.11.2011
Verlag
Springer-Verlag
Erschienen in
Surgical and Radiologic Anatomy / Ausgabe 9/2011
Print ISSN: 0930-1038
Elektronische ISSN: 1279-8517
DOI
https://doi.org/10.1007/s00276-011-0823-9

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