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Dual axonal terminations from the retrosplenial and visual association cortices in the laterodorsal thalamic nucleus of the rat

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Abstract

Light and electron microscopic tracing studies were conducted to assess the synaptic organization in the laterodorsal thalamic nucleus (LD) of the rat and the laminar origins of corticothalamic terminals from the retrosplenial and visual association cortices to LD. A survey of the general ultrastructure of LD revealed at least three types of presynaptic terminals identified on the basis of size, synaptic vesicle morphology, and synaptic membrane specializations: (1) small axon terminals with round synaptic vesicles (SR), which accounted for the majority of terminal profiles and made asymmetric synaptic contacts predominantly with small dendritic shafts and spines; (2) large axon terminals with round synaptic vesicles (LR), which formed asymmetric synaptic contacts mainly with large dendritic shafts; and (3) small to medium-size axon terminals with pleomorphic synaptic vesicles (SMP), which symmetrically synapsed with a wide range of postsynaptic structures from cell bodies to small dendrites. Synaptic glomeruli were identified, whereas no presynaptic dendrites were found. To characterize and identify corticothalamic terminals arising from the retrosplenial and visual association cortices that project to LD, wheat germ agglutinin conjugated to horseradish peroxidase (WGA–HRP) was injected into these cortices. Axons anterogradely labeled with WGA–HRP ended in both SR and LR terminals. On the other hand, dextran-tetramethylrhodamine injected into LD as a retrograde fluorescent tracer labeled large pyramidal cells of layer V as well as small round or multiform cells of layer VI in the retrosplenial and visual association cortices. These findings provide the possibility that corticothalamic terminations from cortical neurons in layer V end as LR terminals, while those from neurons in layer VI end as SR boutons.

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References

  • Bajo VM, Rouiller EM, Welker E, Clarke S, Villa AE, de Ribaupierre Y, de Ribaupierre F (1995) Morphology and spatial distribution of corticothalamic terminals originating from the cat auditory cortex. Hear Res 83:161–174

    Article  PubMed  CAS  Google Scholar 

  • Blair HT, Lipscomb BW, Sharp PE (1997) Anticipatory time interval of head direction cells in the anterior thalamus of the rat: implications for path integration in the head-direction circuit. J Neurophysiol 78:145–159

    Article  PubMed  CAS  Google Scholar 

  • Bourassa J, Pinault D, Deschenes M (1995) Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: a single-fibre study using biocytin as an anterograde tracer. Eur J Neurosci 7:19–30

    Article  PubMed  CAS  Google Scholar 

  • Campbell G, Frost DO (1988) Synaptic organization of anomalous retinal projections to the somatosensory and auditory thalamus: target-controlled morphogenesis of axon terminals and synaptic glomeruli. J Comp Neurol 272:383–408

    Article  PubMed  CAS  Google Scholar 

  • Chen LL, Lin L-H, Green EJ, Barnes CA, McNaughton BL (1994) Head-direction cells in the rat posterior cortex I Anatomical distribution and behavioral modulation. Exp Brain Res 101:8–23

    PubMed  CAS  Google Scholar 

  • Darian-Smith C, Tan A, Edwards S (1999) Comparing thalamocortical and corticothalamic microstructure and spatial reciprocity in the macaque ventral posterolateral nucleus (VPLc) and medial pulvinar. J Comp Neurol 410:211–234

    Article  PubMed  CAS  Google Scholar 

  • Guillery RW (1995) Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. J Anat 187:583–592

    PubMed  Google Scholar 

  • Hoogland HV, Wouterlood FG, Welker E, Van der Loos H (1991) Ultrastructure of giant and small thalamic terminals of cortical origin: a study of the projections from the barrel cortex in mice using Phaseolus vulgaris leucoagglutinin (PHA-L). Exp Brain Res 87:159–172

    Article  PubMed  CAS  Google Scholar 

  • Itaya SK, Van Hoesen GW, Jenq CB (1981) Direct retinal input to the limbic system of the rat. Brain Res 226:33–42

    Article  PubMed  CAS  Google Scholar 

  • Jones EG, Powell TPS (1969) Electron microscopy of synaptic glomeruli in the thalamic relay nuclei of the cat. Proc R Soc Lond B Biol Sci 172:153–171

    Article  PubMed  CAS  Google Scholar 

  • Kakei S, Na J, Shinoda Y (2001) Thalamic terminal morphology and distribution of single corticothalamic axons originating from layers 5 and 6 of the cat motor cortex. J Comp Neurol 437:170–185

    Article  PubMed  CAS  Google Scholar 

  • Kuroda M, Price JL (1991a) Synaptic organization of projections from basal forebrain structures to the mediodorsal thalamic nucleus of the rat. J Comp Neurol 303:513–533

    Article  PubMed  CAS  Google Scholar 

  • Kuroda M, Price JL (1991b) Ultrastructure and synaptic organization of axon terminals from brainstem structures to the mediodorsal thalamic nucleus of the rat. J Comp Neurol 313:539–552

    Article  PubMed  CAS  Google Scholar 

  • Kuroda M, Murakami K, Kishi K, Price JL (1992) Distribution of the piriform cortical terminals to cells in the central segment of the mediodorsal thalamic nucleus of the rat. Brain Res 595:159–163

    Article  PubMed  CAS  Google Scholar 

  • Kuroda M, Yokofujita J, Oda S, Price JL (2004) Synaptic relationships between axon terminals from the mediodorsal thalamic nucleus and γ-aminobutyric acidergic cortical cells in the prelimbic cortex of the rat. J Comp Neurol 477:220–234

    Article  PubMed  CAS  Google Scholar 

  • Ma W, Ohara PT (1987) Synaptic glomeruli in the nucleus submedius of the rat thalamus. Brain Res 415:331–336

    Article  PubMed  CAS  Google Scholar 

  • Mizumori SJY, Williams JD (1993) Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J Neurosci 13:4015–4028

    PubMed  CAS  Google Scholar 

  • Montero VM (1987) Ultrastructural identification of synaptic terminals from the axons of type 3 interneurons in the cat lateral geniculate nucleus. J Comp Neurol 264:268–283

    Article  PubMed  CAS  Google Scholar 

  • Négyessy L, Takács J, Divac I, Hámori J (1994) A combined Golgi and postembedding GABA and glutamate electron microscopic study of the nucleus mediodorsalis thalami of rat. Neurobiology 2:325–341

    PubMed  Google Scholar 

  • Oda S, Kuroda M, Chen SY, Shinkai M, Kishi K (1996) Ultrastructure and distribution of axon terminals from the reticular thalamic nucleus to the anteroventral thalamic nucleus of the rat. J Brain Res 37:459–466

    CAS  Google Scholar 

  • Oda S, Kuroda M, Kakuta S, Tanihata S, Ishikawa Y, Kishi K (2003) Ultrastructure of ascending cholinergic terminals in the anteroventral thalamic nucleus of the rat: a comparison with the mammillothalamic terminals. Brain Res Bull 59:473–483

    Article  PubMed  Google Scholar 

  • Ohara PT, Lieberman AR, Hunt SP, Wu JY (1983) Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat; immunohistochemical studies by light and electron microscopy. Neuroscience 8:189–211

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Ojima H (1994) Terminal morphology and distribution of corticothalamic fibers originating from layers 5 and 6 of cat primary auditory cortex. Cereb Cortex 4:646–663

    Article  PubMed  CAS  Google Scholar 

  • Ojima H, Murakami K, Kishi K (1996) Dual termination modes corticothalamic fibers originating from pyramids of layers 5 and 6 in cat visual cortical area 17. Neurosci Lett 208:57–60

    Article  PubMed  CAS  Google Scholar 

  • Paxinos G, Watson C (1997) The rat brain in stereotaxic coordi-nates. Academic, San Diego

    Google Scholar 

  • Power BD, Mitrofanis J (2001) The zona incerta: substrate for contralateral interconnectivity in the thalamus of rats. J Comp Neurol 436:52–63

    Article  PubMed  CAS  Google Scholar 

  • Robertson RT, Kaitz SS, Robards MJ (1981) A subcortical pathway links sensory and limbic systems of the forebrain. Neurosci Lett 17:161–165

    Article  Google Scholar 

  • Rockland KS (1994) Further evidence for two types of corticopulvinar neurons. Neuroreport 5:1865–1868

    Article  PubMed  CAS  Google Scholar 

  • Rockland KS (1996) Two types of corticopulvinar terminations: round (type 2) and elongate (type 1). J Comp Neurol 368:57–87

    Article  PubMed  CAS  Google Scholar 

  • Rouiller EM, Welker E (1991) Morphology of corticothalamic terminals arising from the auditory cortex of the rat: a Phaseolus vulgaris-leucoagglutinin (PHA-L) tracing study. Hear Res 56:179–190

    Article  PubMed  CAS  Google Scholar 

  • Rouiller EM, Liang F, Moret V, Wiesendanger M (1991) Patterns of corticothalamic terminations following injection of Phaseolus vulgaris leucoagglutinin (PHA-L) in the sensorimotor cortex of the rat. Neurosci Lett 125:93–97

    Article  PubMed  CAS  Google Scholar 

  • Rouiller EM, Tanne J, Moret V, Kermadi I, Boussaoud D, Welker E (1998) Dual morphology and topography of the corticothalamic terminals originating from the primary, supplementary motor, and dorsal premotor cortical areas in macaque monkeys. J Comp Neurol 396:169–185

    Article  PubMed  CAS  Google Scholar 

  • Ryszka A, Heger M (1979) Afferent connections of the laterodorsal thalamic nucleus in the rat. Neurosci Lett 15:61–64

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Shibata H (1998) Organization of projections from rat retrosplenial cortex to the anterior thalamic nuclei in the rat. Eur J Neurosci 10:3210–3219

    Article  PubMed  CAS  Google Scholar 

  • Shibata H (2000) Organization of retrosplenial cortical projections to the laterodorsal thalamic nucleus in the rat. Neurosci Res 38:303–311

    Article  PubMed  CAS  Google Scholar 

  • Spacek J, Lieberman AR (1974) Ultrastructure and three-dimensional organization of synaptic glomeruli in rat somatosensory thalamus. J Anat 117:487–516

    PubMed  CAS  Google Scholar 

  • Sripanidkulchai K, Wyss JM (1986) Thalamic projections to retrosplenial cortex in the rat. J Comp Neurol 254:143–165

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T (1985) The organization of the lateral thalamus of the hooded rat. J Comp Neurol 231:281–309

    Article  PubMed  CAS  Google Scholar 

  • Thompson SM, Robertson RT (1987) Organization of subcortical pathways for sensory projections to the limbic cortex II Afferent projections to the thalamic lateral dorsal nucleus in the rat. J Comp Neurol 265:189–202

    Article  PubMed  CAS  Google Scholar 

  • Van Groen T, Wyss JM (1990) Connections of the retrosplenial granular a cortex in the rat. J Comp Neurol 300:593–606

    Article  PubMed  Google Scholar 

  • Van Groen T, Wyss JM (1992a) Connections of the retrosplenial dysgranular cortex in the rat. J Comp Neurol 315:200–216

    Article  PubMed  Google Scholar 

  • Van Groen T, Wyss JM (1992b) Projections from the laterodorsal nucleus of the thalamus to the limbic and visual cortices in the rat. J Comp Neurol 324:427–448

    Article  PubMed  Google Scholar 

  • Van Groen T, Wyss JM (2003) Connections of the retrosplenial granular b cortex in the rat. J Comp Neurol 463:249–263

    Article  PubMed  Google Scholar 

  • Van Groen T, Vogt BA, Wyss JM (1993) Interconnections between the thalamus and retrosplenial cortex. In: Vogt BA, Gabriel M (eds) Neurobiology of cingulate cortex and limbic thalamus. Birkhåuser, Boston, pp 123–150

    Google Scholar 

  • Wang B, Gonzalo-Ruiz A, Sanz JM, Campbell G, Lieberman AR (1999) Immunoelectron microscopic study of gamma-aminobutyric acid inputs to identified thalamocortical projection neurons in the anterior thalamus of the rat. Exp Brain Res 126:369–382

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The present study was supported in part by Grants-in-Aid for Scientific Research (C) 10680711, 12680739, and 16500229 (to M. Kuroda) from the Ministry of Education, Science, Sports and Culture of Japan. The authors thank Ms. Akane Iijima and Ms. Hiroko Arai for their excellent technical assistance.

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Correspondence to M. Kuroda.

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Shinkai, M., Yokofujita, J., Oda, S. et al. Dual axonal terminations from the retrosplenial and visual association cortices in the laterodorsal thalamic nucleus of the rat. Anat Embryol 210, 317–326 (2005). https://doi.org/10.1007/s00429-005-0047-z

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