Striatal projections from the rat lateral posterior thalamic nucleus

The dorsocentral striatum (DCS) has been implicated as an associative striatal area receiving inputs from several cortical areas including medial agranular cortex (AGm), posterior parietal cortex (PPC), and visual association cortex to form a cortical-subcortical circuit involved in directed attention and neglect. The lateral posterior thalamic nucleus (LP) may also play a role in directed attention and neglect because LP has robust reciprocal connections with these cortical areas and projects to DCS. We used anterograde axonal tracing to map thalamostriatal projections from LP and surrounding thalamic nuclei, with a focus on projections to DCS. The thalamic nuclei investigated included LP, laterodorsal thalamic nucleus (LD), central lateral nucleus (CL), and posterior thalamic nucleus (Po). We found that the mediorostral part of LP (LPMR) projects strongly to DCS as well as to the dorsal peripheral region of the striatum. Further, there is topography within LPMR and DCS such that the far medial LPMR projects to the central region of DCS (projection area of AGm) and the central LPMR projects to the dorsal region of DCS (projection area of PPC and Oc2M). In contrast, the laterorostral part of LP (LPLR) and other thalamic nuclei surrounding LP project to dorsolateral to dorsomedial peripheral regions of the striatum but do not project to DCS. These findings indicate that DCS is a region of convergence for thalamostriatal and corticostriatal projections from regions that are themselves interconnected, serving as the key element of the corticostriatal-thalamic network mediating spatial processing and directed attention.

[1]  J. Veening,et al.  The topical organization of the afferents to the caudatoputamen of the rat. A horseradish peroxidase study , 1980, Neuroscience.

[2]  Atsutaka Hashimoto,et al.  Afferent connections of medial precentral cortex in the rat , 1984, Neuroscience Letters.

[3]  P. Goldman-Rakic,et al.  Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  J. Lanciego,et al.  Re-examination of the thalamostriatal projections in the rat with retrograde tracers , 2002, Neurosciences research.

[5]  R. Reep,et al.  Topographic organization of the striatal and thalamic connections of rat medial agranular cortex , 1999, Brain Research.

[6]  R. Reep,et al.  Overlap and interdigitation of cortical and thalamic afferents to dorsocentral striatum in the rat , 2005, Brain Research.

[7]  J. Lanciego,et al.  A re-examination of the striatal input from the mediodorsal thalamic nucleus in the rat , 2000 .

[8]  C. Gerfen The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination. , 1989, Science.

[9]  M. Gallagher,et al.  Thalamic and basal forebrain cholinergic connections of the rat posterior parietal cortex. , 1999, Neuroreport.

[10]  N. Mizuno,et al.  Distribution of thalamo-caudate neurons in the cat as demonstrated by horseradish peroxidase , 1979, Experimental Brain Research.

[11]  C. Gerfen The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems , 1984, Nature.

[12]  A. D. Smith,et al.  The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones , 1990, Trends in Neurosciences.

[13]  R. L. Reep,et al.  Rat posterior parietal cortex: topography of corticocortical and thalamic connections , 2004, Experimental Brain Research.

[14]  S. D. L. Heras,et al.  Striatal projections from the lateral and posterior thalamic complexes. An anterograde tracer study in the cat , 2006, Histochemistry and Cell Biology.

[15]  R. Reep,et al.  Layer VII and the gray matter trajectories of corticocortical axons in rats , 1996, Anatomy and Embryology.

[16]  R. Reep,et al.  Rodent posterior parietal cortex as a component of a cortical network mediating directed spatial attention , 1998, Psychobiology.

[17]  C. Wilson,et al.  Corticostriatal innervation of the patch and matrix in the rat neostriatum , 1996, The Journal of comparative neurology.

[18]  A. Mcgeorge,et al.  The organization and collateralization of corticostriate neurones in the motor and sensory cortex of the rat brain , 1987, Brain Research.

[19]  M. F. Huerta,et al.  Differential thalamic connectivity of rostral and caudal parts of cortical area Fr2 in rats , 1991, Brain Research.

[20]  R. Reep,et al.  Infusion of apomorphine into the dorsocentral striatum produces acute drug-induced recovery from neglect produced by unilateral medial agranular cortex lesions in rats , 2003, Behavioural Brain Research.

[21]  J. Lanciego,et al.  Striatal input from the ventrobasal complex of the rat thalamus , 2001, Histochemistry and Cell Biology.

[22]  R. T. Watson,et al.  Efferent Connections of the Rostral Portion of Medial Agranular Cortex in Rats , 1987, Brain Research Bulletin.

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

[24]  P. Goldman-Rakic Cytoarchitectonic heterogeneity of the primate neostriatum: Subdivision into island and matrix cellular compartments , 1982, The Journal of comparative neurology.

[25]  R. Reep,et al.  Topographic organization in the corticocortical connections of medial agranular cortex in rats , 1990, The Journal of comparative neurology.

[26]  J. Corwin,et al.  Neglect following unilateral ablation of the caudal but not the rostral portion of medial agranular cortex of the rat and the therapeutic effect of apomorphine , 1990, Behavioural Brain Research.

[27]  W. Nauta,et al.  An intricately patterned prefronto‐caudate projection in the rhesus monkey , 1977, The Journal of comparative neurology.

[28]  H. Groenewegen,et al.  Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat , 1991, Neuroscience.

[29]  K. Sukekawa Reciprocal connections between medial prefrontal cortex and lateral posterior nucleus in rats. , 1988, Brain, behavior and evolution.

[30]  G. Paxinos The Rat nervous system , 1985 .

[31]  K. Heilman,et al.  Apomorphine has a therapeutic effect on neglect produced by unilateral dorsomedial prefrontal cortex lesions in rats , 1986, Experimental Neurology.

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

[33]  G. V. Van Hoesen,et al.  Widespread corticostriate projections from temporal cortex of the rhesus monkey , 1981, The Journal of comparative neurology.

[34]  H. Groenewegen,et al.  Nuclear origin of thalamic afferents of the ventral striatum determines their relation to patch/matrix configurations in enkephalin-immunoreactivity in the rat. , 1988, Journal of chemical neuroanatomy.

[35]  R. Reep,et al.  The associative striatum: Organization of cortical projections to the dorsocentral striatum in rats , 2003, The Journal of comparative neurology.

[36]  R. Reep,et al.  Neuronal connections of orbital cortex in rats: topography of cortical and thalamic afferents , 1996, Experimental Brain Research.

[37]  Prof. Dr. Karl Zilles The Cortex of the Rat , 1985, Springer Berlin Heidelberg.

[38]  R. L. Reep,et al.  Thalamocortical connections of rat posterior parietal cortex , 1992, Neuroscience Letters.

[39]  N. Mizuno,et al.  Topographical projections from the thalamus to the putamen in the cat , 1985, Neuroscience Letters.

[40]  A. M. Graybiel,et al.  Compartmental origins of striatal efferent projections in the cat , 1989, Neuroscience.

[41]  R. Reep,et al.  Unilateral destruction of the dorsocentral striatum in rats produces neglect but not extinction to bilateral simultaneous stimulation , 2002, Behavioural Brain Research.

[42]  Charles J. Wilson,et al.  Connectivity and Convergence of Single Corticostriatal Axons , 1998, The Journal of Neuroscience.

[43]  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.

[44]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[45]  M. J. Christie,et al.  Excitatory amino acid projections to the nucleus accumbens septi in the rat: A retrograde transport study utilizingd[3H]aspartate and [3H]GABA , 1987, Neuroscience.

[46]  E. Yeterian,et al.  Cortico-striate projections in the rhesus monkey: The organization of certain cortico-caudate connections , 1978, Brain Research.

[47]  N. Mizuno,et al.  Topographical projections from the posterior thalamic regions to the striatum in the cat, with reference to possible tecto-thalamo-striatal connections , 2004, Experimental Brain Research.

[48]  O. Phillipson,et al.  The topographic order of inputs to nucleus accumbens in the rat , 1985, Neuroscience.

[49]  R. Reep,et al.  The associative striatum: cortical and thalamic projections to the dorsocentral striatum in rats , 2003, Brain Research.

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

[51]  J. Corwin,et al.  Comparisons of hemi-inattention produced by unilateral lesions of the posterior parietal cortex or medial agranular prefrontal cortex in rats Neglect, extinction, and the role of stimulus distance , 1993, Behavioural Brain Research.

[52]  R. Reep,et al.  Unilateral destruction of the medial agranular cortical projection zone in the dorsocentral striatum produces severe neglect in rats , 2000, Psychobiology.

[53]  Terry T. Takahashi,et al.  The organization of the lateral thalamus of the hooded rat , 1985, The Journal of comparative neurology.

[54]  H. Nauta,et al.  Afferents to the rat caudoputamen studied with horseradish peroxidase. An evaluation of a retrograde neuroanatomical research method. , 1974, Brain research.

[55]  André Parent,et al.  Two different types of thalamic fibers innervate the rat striatum , 1995, Brain Research.

[56]  M. Takada The lateroposterior thalamic nucleus and substantia nigra pars lateralis: Origin of dual innervation over the visual system and basal ganglia , 1992, Neuroscience Letters.

[57]  M. Norita,et al.  The organization of the thalamostriatal projection from the lateral posterior thalamic nuclear complex (LP) in the pigmented rat. , 1998, Neurobiology.

[58]  Leonidas D. Iasemidis,et al.  Quantitative Neuroscience: Models, Algorithms, Diagnostics, and Therapeutic Applications , 2004 .

[59]  J. Corwin,et al.  Spatial deficits and hemispheric asymmetries in the rat following unilateral and bilateral lesions of posterior parietal or medial agranular cortex , 1992, Behavioural Brain Research.

[60]  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.

[61]  M. Schwab,et al.  Nogo-A inhibition induces recovery from neglect in rats , 2008, Behavioural Brain Research.