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Reevaluation of synaptic relationships of cerebellar terminals in the ventral lateral nucleus of the rhesus monkey thalamus based on serial section analysis and three-dimensional reconstruction

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Abstract

Terminals of cerebellar afferents (CB) to different regions of the ventral lateral nucleus (VL) of the rhesus monkey thalamus were labeled with wheat germ agglutinin-horseradish peroxidase following injections into the dentate nucleus. Synaptic relationships of 17 CB with projection neuron dendrites (PNd) and local circuit neuron dendrites (LCNd) were analyzed in serial ultrathin sections from dorsal and ventral VL regions, which are known to differ cytoarchitecturally and functionally. Three terminals were reconstructed using three-dimensional (3D) computer image analysis techniques to obtain volumetric and planar measurements. CB in the ventral VL were often flat and elongated with synaptic vesicles arranged in clusters. Each CB was engaged with one PNd and one to four LCNd. A single bouton formed 8–50 synaptic contacts, with those on PNd outnumbering the ones on LCNd 4.1∶1. Only some CB in the ventral VL were engaged in complex synaptic arrangements such as triads and serial synapses. Most CB in the dorsal VL displayed a roundish shape and numerous uniformly distributed synaptic vesicles. They formed 5–25 synaptic contacts with a 3∶1 ratio of contacts on PNd compared with those on LCNd. CB in the dorsal VL participated in a variety of complex synaptic arrangements. Two types of triads were found: classic with CB, PNd and LCNd, and unconventional with CB and two LCNd. CB were also involved in serial synapses with two LCNd or LCNd and another PNd, and serial sequential synapses with two LCNd and a PNd. Three glomerulus-like structures were encountered in the dorsal VL. 3D reconstruction and volumetric measurements revealed that synaptic contacts formed by CB on PNd had varying shapes and sizes (0.022–0.274 μm2). Synapses formed on LCNd were larger (0.09–0.407 μm2). The total area of all active zones of a single CB on LCNd was either equal to or about 40% smaller than that of synapses on PNd. The entire active zone area comprised 1–1.6% of the total CB surface area and did not seem to correlate with the volume. Synaptic contacts formed by associated LCNd on PNd in complex arrangements were usually small (0.021–0.044 μm2). The results suggest that: synapses formed by CB on PNd and LCNd, and synapses formed by LCNd on PNd may differ in strength; a variety of different circuits participate in the processing of cerebellar afferent information in the primate VL; and these circuits differ in functionally different VL subdivisions.

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References

  • Anderson ME, Turner RS (1991) Activity of neurons in cerebellar-receiving and pallidal-receiving areas of the thalamus of the behaving monkey. J Neurophysiol 66:879–893

    Google Scholar 

  • Angaut P (1970) The ascending projection of the nucleus interpositus posterior of the cat cerebellum: an experimental anatomical study using silver impregnation methods. Brain Res 24:337–394

    Google Scholar 

  • Angaut P, Bowsher D (1970) Ascending projection of the medial cerebellar (fastigial) nucleus: an experimental study in cat. Brain Res 24:49–68

    Google Scholar 

  • Asanuma C, Thach WT, Jones EG (1983) Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey. Brain Res Brain Res Rev 5:237–265

    Google Scholar 

  • Cook LT (1980) An algorithm for volume estimation based on polyhedral approximation. IEEE Trans Biomed Eng 9:493–499

    Google Scholar 

  • Desmond NL, Levy WB (1988) Synaptic interface surface area increases with long-term potentiation in the hippocampal dentate gyms. Brain Res 453:308–314

    Google Scholar 

  • Famiglietti EV, Peters A (1972) The synaptic glomerulus and intrinsic neurons in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 144:285–334

    Google Scholar 

  • Faull RLM, Mehler WR (1978) The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projections in the rat. Neuroscience 3:989–1002

    Google Scholar 

  • Foley JD, Van Dam A, Feiner SK, Hughes JF (1990) Computer graphics principles and practice. Addison-Wesley, Reading, MA

    Google Scholar 

  • Ganapathy S (1982) New general triangulation method for planar contours. Comp Graphics 16:69–75

    Article  CAS  Google Scholar 

  • Guillery RW (1969) The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus in the cat. Z Zellforsch 96:1–38

    Google Scholar 

  • Hamori J, Pasik T, Pasik P, Szentagothai J (1974) Triadic synaptic arrangements and their possible significance in the lateral geniculate nucleus of the monkey. Brain Res 80:379–393

    Google Scholar 

  • Hamos JE, Van Horn SC, Raczkowski D, Ulrich DJ, Sherman SM (1985) Synaptic connectivity of a local circuit neurons in lateral geniculate of the cat. Nature 317:618–621

    Google Scholar 

  • Harding BN (1973) An ultrastructural study of the termination of afferent fibres within the ventrolateral nuclei of the monkey thalamus. Brain Res 54:341–346

    Google Scholar 

  • Harding BN, Powell TPS (1977) An electron microscopic study of the centre median and ventrolateral nuclei of the thalamus in the monkey. Philos Trans R Soc Lond [Biol] 279:359–412

    Google Scholar 

  • Hendry SHC, Jones EG, Graham J (1979) Thalamic relay nuclei and certain related fiber systems in cat. J Comp Neurol 185:679–714

    Google Scholar 

  • Hillman DE, Chen S (1984) Reciprocal relationship between size of postsynaptic densities and their number: constancy in contact area. Brain Res 295:325–343

    Google Scholar 

  • Hillman DE, Chen S (1985) Compensation in the number of presynaptic dense projections and synaptic vesicles in remaining paralell fibers following cerebellar lesion. J Neurocytol 14:673–687

    Google Scholar 

  • Houser CR, Vaughn JE, Barber RP, Roberts E (1980) GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res 200:341–354

    Google Scholar 

  • Ilinsky IA, Kultas-Ilinsky K (1982) Stereotactic surgery in the rhesus monkey (Macaca mulatta) utilizing intracerebral landmarks. Appl Neurophysiol 45:563–572

    Google Scholar 

  • Ilinsky IA, Kultas-Ilinsky K (1984) An autoradiographic study of the topographical relationships between the pallidal and cerebellar projections to the cat thalamus. Exp Brain Res 54:95–106

    Google Scholar 

  • Ilinsky IA, Kultas-Ilinsky K (1987) Sagittal cytoarchitechtonic maps of the Macaca mulatta thalamus with a revised nomenclature of the motor-related nuclei validated by observation on their connectivity. J Comp Neurol 262:331–364

    Google Scholar 

  • Ilinsky IA, Kultas-Ilinsky K (1990) Fine structure of the magnocellular subdivision of the ventral anterior thalamic nucleus (VAmc) of Macaca mulatta: cell types and synaptology. J Comp Neurol 294:455–478

    Google Scholar 

  • Ilinsky IA, Toga AW, Kultas-Ilinsky K (1993) Anatomical organization of internal neuronal ircuits in the motor thalamus. In: Minciacchi D, Molinari M, Macchi G, Jones EG (eds) Thalamic networks for relay and modulation. Pergamon, Oxford, pp 155–164

    Google Scholar 

  • Jansen J, Jansen J (1955) On the efferent fibers of the cerebellar nuclei in the cat. J Comp Neurol 102:607–632

    Google Scholar 

  • Jones EG (1985) The thalamus. Plenum, Oxford

    Google Scholar 

  • Kalil K (1981) Projections of the cerebellar and dorsal column nuclei upon the thalamus of the rhesus monkey. J Comp Neurol 195:25–50

    CAS  Google Scholar 

  • Koch C (1985) Understanding the intrinsic circuitry of the cat's lateral geniculate nucleus: electrical properties of the spine-triad arrangement. Proc R Soc Lond [Biol] 225:365–390

    Google Scholar 

  • Kullman DM, Nicoll RA (1992) Long-term potentiation is associated with increase in quantal content and quantal amplitude. Nature 357:240–244

    Google Scholar 

  • Kultas-Ilinsky K, Ilinsky IA (1986) Neuronal and synaptic organization of the motor nuclei of mammalian thalamus. In: Jones DG (ed) Current topics in research on synapses, vol 3. Liss, New York, pp 77–145

    Google Scholar 

  • Kultas-Ilinsky K, Ilinsky IA (1991) Fine structure of the ventral lateral nucleus (VL) of the Macaca mulatta thalamus: cell types and synaptology. J Comp Neurol 314:319–349

    Google Scholar 

  • Kultas-Ilinsky K, Ilinsky IA, Young PA, Smith KR (1980a) Ultratructure of degenerating cerebellothalamic terminals in the ventral medial nucleus of the cat. Exp Brain Res 38:125–135

    Google Scholar 

  • Kultas-Ilinsky K, Warton S, Tolbert DL, Ilinsky IA (1980b) Quantitative and qualitative characteristics of dentate and fastigial afferents identified by electron microscopic autoradiography in the cat thalamus. Brain Res 201:220–226

    Google Scholar 

  • Kultas-Ilinsky K, Ribak CE, Peterson GM, Oertel WH (1985) A description of the GABAergic neurons and axons terminals in the motor nuclei of the cat thalamus. J Neurosci 5:1346–1369

    Google Scholar 

  • Kultas-Ilinsky K, Yi H, Ilinsky IA (1995) Nucleus reticularis input to the anterior thalamic nuclei in the monkey: a light and electron microscopic study. Neurosci Lett 186:25–28

    Google Scholar 

  • Mason A, Beck S, Yi H, Kultas-Ilinsky K, Ilinsky IA (1993) Synaptic relationships of cerebellar afferent terminals in the monkey thalamus studied in serial sections and 3D reconstructions. Soc Neurosci Abstr 19:1436

    Google Scholar 

  • Mesulam M (1976) The blue reaction product in horseradish peroxidase neurohistochemistry: incubation parameters and visibility. J Histochem Cytochem 24:1273–1280

    Google Scholar 

  • Morest DK (1971) Dendrodendritic synapses of cells that have axons: the fine structure of the Golgi type II cell in the medial geniculate body of the cat. Z Anat Entwickl Gesch 133:216–246

    Google Scholar 

  • Nieoullon A, Kerkerian L, Dusticier N (1984) High affinity glutamate uptake in the red nucleus and ventrolateral thalamus after lesion of the cerebellum in adult cat. Exp Brain Res 55:409–419

    Google Scholar 

  • Ohara PT, Lieberman AR (1993) Some aspects of the synptic circuitry underlying inhibition in the ventrobasal thalamus. J Neurocytol 22:815–825

    Google Scholar 

  • Ohara PT, Chazal G, Ralston HJ III (1989) Ultrastructural analysis of GABA-immunoreactive elements in the monkey thalamic ventrobasal complex. J Comp Neurol 283:541–558

    Google Scholar 

  • Olszewski J (1952) The thalamus of Macaca mulatta. An atlas for use with stereotaxic instrument. Karger, Basel

    Google Scholar 

  • Olucha F, Martinez-Garcia F, Lopez-Garcia C (1985) A new stabilizing agent for the tetramethylbenzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase (HRP). J Neurosci Methods 13:131–138

    Google Scholar 

  • Percheron G (1977) The thalamic territory of cerebellar afferents and the lateral region of the thalamus of the macaque in stereotaxic ventricular coordinates. J Hirnforsch 18:375–400

    Google Scholar 

  • Pierce JP, Lewin GR (1994) An ultrastructural size principle. Neuroscience 58:441–446

    Google Scholar 

  • Propst JW, Ko CP (1987) Correlation between active zone ultrastructure and synaptic function studied with freeze-fracture of physiologically identified neuromuscular junctions. J Neurosci 7:3654–3664

    Google Scholar 

  • Purves D, Voyvodic JT, Magrassi L, Yawo H (1987) Nerve terminal remodeling visualized in living mice by repeated examination of the same neuron. Science 238:1122–1126

    Google Scholar 

  • Ralston HJ III (1971) Evidence for presynaptic dendrites and proposal for their mechanism of action. Nature 230:585–587

    Google Scholar 

  • Ralston HJ III (1985) The fine structure of the ventrobasal thalamus of the monkey and cat. Brain Res Rev 9:228–241

    Google Scholar 

  • Ralston HJ III, Ralston DD (1994) Medial lemniscal and spinal projections to the Macaque thalamus: an electron microscopic study of differing GABAergic circuitry serving thalamic somatosensory mechanisms. J Neurosci 14 (5):2485–2502

    Google Scholar 

  • Rapisardi SC, Miles TP (1984) Synaptology of retinal terminals in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 223:515–534

    Google Scholar 

  • Rinvik E, Grofova I (1974a) Light and electron microscopical studies ot the normal nuclei ventralis lateralis and ventralis anterior thalami. Anat Embryol 146:57–93

    Google Scholar 

  • Rinvik E, Grofova I (1974b) Cerebellar projections to the nuclei ventralis lateralis and ventralis anterior thalami. Anat Embryol 146:95–111

    Google Scholar 

  • Rispal-Padel L, Grangetto A (1977) The cerebello-thalamo cortical pathway. Topographical investigation at the unitary level in cat. Exp Brain Res 28:101–123

    Google Scholar 

  • Sawyer SF, Martone ME, Groves PM (1991) A GABA immunocytochemical study of rat motor thalamus: light and electron microscopic observation. Neuroscience 42:103–124

    Google Scholar 

  • Schwartz ML, Dekker JJ, Goldman-Rakic PS (1991) Dual mode of corticothalamic synaptic termination in the mediodorsal nucleus of the Rhesus monkey. J Comp Neurol 309:289–304

    Google Scholar 

  • Sherman SM, Koch C (1986) The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Exp Brain Res 63:1–20

    Google Scholar 

  • Shinoda Y, Futami T, Kano M (1985) Synaptic organization of cerebello-thalamo-cerebral parthway in the cat. II. Input-output organization of single thalamo-cortical neurons in the ventrolateral thalamus. Neurosci Res 2:157–180

    Google Scholar 

  • Stanton GB (1980) Topographical organization of ascending cerebellar projections from th edentate and interposed nuclei in macaca mulatta: an anterograde degeneration study. J. Comp Neurol 190:699–731

    Google Scholar 

  • Strick PL (1976) Anatomical analysis of ventrolateral thalamic input to primate motor cortex. J Neurophysiol 39:1020–1031

    Google Scholar 

  • Tai Y, Yi H, Ilinsky IA, Kultas-Ilinsky K (1995) Nucleus reticularis thalami connections with the mediodorsal nucleus: a light and electron microscopic study in the monkey. Brain Res Bull 38:475–488

    Google Scholar 

  • Vahle-Hinz C, Hicks TP, Gottschaldt K-M (1994) Aminoacids modify thalamocortical response transformation expressed by neurons of the ventrobasal complex. Brain Res 637:139–155

    Google Scholar 

  • Vitek FL, Ashe J, DeLong M, Alexander GE (1994) Physiologic properties and somatotopic organization of the primate motor thalamus. J Neurophysiol 71:1498–1513

    Google Scholar 

  • Uno M, Yoshida M, Hirota I (1970) The mode of cerebellothalamic relay transmission investigated with intracellular recording from cells of the ventrolateral nucleus of cat's thalamus. Exp Brain Res 10:121–139

    Google Scholar 

  • Yamamoto t, Noda T, Samejima A, Oka H (1988) Electrophysiological and morphological features of thalamic neurons with special reference to the cerebellar and pallidal inputs. In: Bentivoglio M, Spreafico R (eds) Cellular thalamic mechanisms. Elsevier, Amsterdam, pp 239–260

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, University of Iowa College of Medicine, 52242, Iowa City, IA, USA

    Alicja Mason, Igor A. Ilinsky & Kristy Kultas-Ilinsky

  2. Image Analysis Facility, University of Iowa College of Medicine, 52242, Iowa City, IA, USA

    Steven Beck

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  1. Alicja Mason
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  4. Kristy Kultas-Ilinsky
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Mason, A., Ilinsky, I.A., Beck, S. et al. Reevaluation of synaptic relationships of cerebellar terminals in the ventral lateral nucleus of the rhesus monkey thalamus based on serial section analysis and three-dimensional reconstruction. Exp Brain Res 109, 219–239 (1996). https://doi.org/10.1007/BF00231783

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