A Single‐cell Study of the Axonal Projections Arising from the Posterior Intralaminar Thalamic Nuclei in the Rat

Thalamostriatal projections arising from the posterior intralaminar nuclei (Pl; the parafascicular nucleus and the adjacent caudalmost part of the posterior thalamic group) were studied in rats by tracing the axons of small pools of neurons labelled anterogradely with biocytin. Thirteen Pl cells were also stained by juxtacellular application of the tracer. Relay cells of Pl nuclei have a morphology that differs radically from the classical descriptions of the bushy cells which represent the main neuronal type of the sensory thalamic relay nuclei. Pl cells have ovoid or polygonal somata of ˜20–25 μm, from which emerge four or five thick, long and poorly branched dendrites bearing spines and filamentous appendages; their dendritic domains extend for up to 1.5 mm. Before leaving the nucleus 20% of axons give off collaterals that ramify locally. All axons course through the thalamic reticular nucleus, where they emit one or two poorly branched collaterals, traverse the globus pallidus, where they also distribute collaterals, and arborize massively in the striatum and sparsely in the cerebral cortex. At the striatal level four or five collaterals leave the main axon and terminate in patches scattered dorsoventrally within a rostrocaudally oriented slab. As revealed by calbindin D‐28k immunohistochemistry, only the matrix compartment receives terminations from Pl axons. The cortical branch forms small terminal puffs centred upon layer VI of the motor cortex. Before entering the striatum some axons of the parafascicular nucleus give rise to descending collaterals that arborize in the entopeduncular nucleus, in the subthalamic nucleus and in the vicinity of the red nucleus. Other axons arising from the caudal part of the posterior group send descending branches only to the entopeduncular nucleus. These findings show that Pl cells belong to a distinct category of thalamic relay neurons which, beside their massive projection to the striatum, also distribute collaterals to other components of the basal ganglia. Moreover, these results provide the first direct evidence that virtually all Pl cells project to both striatum and cerebral cortex. Finally, it is proposed on the basis of morphological, histochemical and hodological criteria that the caudal part of the posterior thalamic group in the rat is homologous to the suprageniculate‐limitans nuclei of cats and primates.

[1]  R. Hevner,et al.  A metabolic map of cytochrome oxidase in the rat brain: Histochemical, densitometric and biochemical studies , 1995, Neuroscience.

[2]  B. Hu Cellular basis of temporal synaptic signalling: an in vitro electrophysiological study in rat auditory thalamus. , 1995, The Journal of physiology.

[3]  M. Deschenes,et al.  Corticothalamic Projections from the Cortical Barrel Field to the Somatosensory Thalamus in Rats: A Single‐fibre Study Using Biocytin as an Anterograde Tracer , 1995, The European journal of neuroscience.

[4]  H. Groenewegen,et al.  The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei , 1994, Trends in Neurosciences.

[5]  M. Bevan,et al.  The projections from the parafascicular thalamic nucleus to the subthalamic nucleus and the striatum arise from separate neuronal populations: A comparison with the corticostriatal and corticosubthalamic efferents in a retrograde fluorescent double-labelling study , 1994, Neuroscience.

[6]  D. Pinault Golgi-like labeling of a single neuron recorded extracellularly , 1994, Neuroscience Letters.

[7]  J. Crabtree The Somatotopic Organization Within the Cat's Thalamic Reticular Nucleus , 1992, The European journal of neuroscience.

[8]  J. Crabtree,et al.  The Somatotopic Organization Within the Rabbit's Thalamic Reticular Nucleus , 1992, The European journal of neuroscience.

[9]  A. Parent,et al.  Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: A light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity , 1992, The Journal of comparative neurology.

[10]  A. Parent,et al.  Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: A PHA‐L study of subcortical projections , 1992, The Journal of comparative neurology.

[11]  M. Conley,et al.  The Organization of Projections from Subdivisions of the Auditory Cortex and Thalamus to the Auditory Sector of the Thalamic Reticular Nucleus in Galago , 1991, The European journal of neuroscience.

[12]  C. W. Ragsdale,et al.  Compartmental organization of the thalamostriatal connection in the cat , 1991, The Journal of comparative neurology.

[13]  M. Celio,et al.  Calbindin D-28k and parvalbumin in the rat nervous system , 1990, Neuroscience.

[14]  H. Groenewegen,et al.  Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum , 1990, The Journal of comparative neurology.

[15]  Michael Conley,et al.  Organization of the Visual Sector of the Thalamic Reticular Nucleus in Galago , 1990, The European journal of neuroscience.

[16]  A. Parent,et al.  The centre me´dian and parafascicular thalamic nuclei project respectively to the sensorimotor and associative-limbic striatal territories in the squirrel monkey , 1990, Brain Research.

[17]  H. Killackey,et al.  The Topographic Organization and Axis of Projection within the Visual Sector of the Rabbit's Thalamic Reticular Nucleus , 1989, The European journal of neuroscience.

[18]  J. Winer,et al.  A cytoarchitectonic atlas of the medial geniculate body of the opossum, Didelphys virginiana, with a comment on the posterior intralaminar nuclei of the thalamus , 1988, The Journal of comparative neurology.

[19]  G. J. Royce,et al.  A Golgi and ultrastructural analysis of the centromedian nucleus of the cat , 1986, The Journal of comparative neurology.

[20]  A. Jayaraman,et al.  The projection pattern of the suprageniculate nucleus to the caudate nucleus in cats , 1986, Brain Research.

[21]  G. J. Royce,et al.  Efferent connections of the centromedian and parafascicular thalamic nuclei: An autoradiographic investigation in the cat , 1985, The Journal of comparative neurology.

[22]  A. Parent,et al.  Midbrain tegmental projections of nucleus reticularis thalami of cat and monkey: A retrograde transport and antidromic invasion study , 1984, The Journal of comparative neurology.

[23]  R. M. Beckstead A projection to the striatum from the medial subdivision of the posterior group of the thalamus in the cat , 1984, Brain Research.

[24]  R. Llinás,et al.  Electrophysiological properties of guinea‐pig thalamic neurones: an in vitro study. , 1984, The Journal of physiology.

[25]  R. M. Beckstead The thalamostriatal projection in the cat , 1984, The Journal of comparative neurology.

[26]  J. Winer,et al.  The medial division of the medial geniculate body of the cat: implications for thalamic organization , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  A. Parent,et al.  The subcortical afferents to caudate nucleus and putamen in primate: A fluorescence retrograde double labeling study , 1983, Neuroscience.

[28]  G. J. Royce Single thalamic neurons which project to both the rostral cortex and caudate nucleus studied with the fluorescent double labeling method , 1983, Experimental Neurology.

[29]  T. Hattori,et al.  Direct projections from the centre median‐parafascicular complex to the subthalamic nucleus in the cat and rat , 1983, The Journal of comparative neurology.

[30]  M Steriade,et al.  Neocortical and caudate projections of intralaminar thalamic neurons and their synaptic excitation from midbrain reticular core. , 1982, Journal of neurophysiology.

[31]  K. Jinnai,et al.  Thalamocaudate projection neurons with a branching axon to the cerebral motor cortex , 1981, Neuroscience Letters.

[32]  M. J. Friedlander,et al.  Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. , 1981, Journal of neurophysiology.

[33]  M. Herkenham,et al.  Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum , 1981, Nature.

[34]  D. Kooy,et al.  The organization of the efferent projections and striatal afferents of the entopeduncular nucleus and adjacent areas in the rat , 1981, Brain Research.

[35]  B. Berger,et al.  Double labelling of branched neurons in the central nervous system of the rat by retrograde axonal transport of horseradish peroxidase and iron dextran complex , 1979, Neuroscience Letters.

[36]  M. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

[37]  G. J. Royce Autoradiographic evidence for a discontinuous projection to the caudate nucleus from the centromedian nucleus in the cat , 1978, Brain Research.

[38]  G. Macchi,et al.  The cortical projections of the thalamic intralaminar nuclei restudied by means of the HRP retrograde axonal transport , 1977, Neuroscience Letters.

[39]  C. Fox,et al.  The neurons in the centromedian‐parafascicular complex of the monkey (Macaca mulatta): A Golgi Study , 1976, The Journal of comparative neurology.

[40]  E. Jones,et al.  Retrograde axonal transport and the demonstration of non‐specific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey , 1974, The Journal of comparative neurology.

[41]  D. Albe-Fessard,et al.  Projections of medial thalamic nuclei to putamen and cerebral frontal cortex in the cat. , 1973, Brain research.

[42]  A. Scheibel,et al.  Structural organization of nonspecific thalamic nuclei and their projection toward cortex. , 1967, Brain research.

[43]  R. Lund,et al.  Thalamic afferents from the spinal cord and trigeminal nuclei. An experimental anatomical study in the rat. , 1967, The Journal of comparative neurology.

[44]  J. W. Papez The thalamic nuclei of the nine‐banded armadillo (tatusia novemcincta) , 1932 .

[45]  M. Bentivoglio,et al.  The specificity of the nonspecific thalamus: the midline nuclei. , 1991, Progress in brain research.

[46]  G. J. Royce Recent Research on the Centromedian and Parafascicular Nuclei , 1987 .

[47]  M. Herkenham,et al.  New Perspectives on the Organization and Evolution of Nonspecific Thalamocortical Projections , 1986 .

[48]  E. Jones Functional subdivision and synaptic organization of the mammalian thalamus. , 1981, International review of physiology.

[49]  D. Carter,et al.  The projections of the entopeduncular nucleus and globus pallidus in rat as demonstrated by autoradiography and horseradish peroxidase histochemistry , 1978, The Journal of comparative neurology.

[50]  H. Kuhlenbeck The human diencephalon; a summary of development, structure, function, and pathology. , 1954, Confinia neurologica.

[51]  H. Jasper,et al.  Diffuse projection systems: the integrative action of the thalamic reticular system. , 1949, Electroencephalography and clinical neurophysiology.