The associative striatum: Organization of cortical projections to the dorsocentral striatum in rats

The dorsocentral striatum (DCS) is the major site of input from medial agranular cortex (AGm) and has been implicated as an associative striatal area that is part of a cortical‐subcortical circuit involved in multimodal spatial functions involving directed attention. Anterograde axonal tracing was used to investigate the spatial organization of corticostriatal projections to DCS. Injections of biotinylated dextran amine were made into several cortical areas known to project to DCS based on retrograde tracing data. These included areas AGm, lateral agranular cortex (AGl), orbital cortex, posterior parietal cortex (PPC), and visual association cortex. We discovered a previously undescribed geometry whereby the projection from AGm is prominent within DCS and the main corticostriatal projections from areas other than AGm are situated around the periphery of DCS: visual association cortex dorsomedially, PPC dorsally, AGl laterally, and orbital cortex ventrally. Each of these cortical projections is also represented by less dense aggregates of terminal labeling within DCS, organized as focal patches and more diffuse labeling. Because these cortical areas are linked by corticocortical connections, the present findings indicate that interconnected cortical areas have convergent terminal fields in the region of DCS. These findings suggest that DCS is a central associative region of the dorsal striatum characterized by a high degree of corticostriatal convergence. J. Comp. Neurol. 467:271–292, 2003. © 2003 Wiley‐Liss, Inc.

[1]  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.

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

[3]  R. Reep,et al.  Effects of light deprivation on recovery from neglect and extinction induced by unilateral lesions of the medial agranular cortex and dorsocentral striatum , 2003, Behavioural Brain Research.

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

[5]  C. Wilson,et al.  Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. , 1994, Journal of neurophysiology.

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

[7]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[8]  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.

[9]  M. Roger,et al.  Topographical organization of the projections from physiologically identified areas of the motor cortex to the striatum in the rat , 1992, Neuroscience Research.

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

[11]  M. Deschenes,et al.  Corticothalamic projections from layer V cells in rat are collaterals of long-range corticofugal axons , 1994, Brain Research.

[12]  C. Saper,et al.  Efferent projections of the infralimbic cortex of the rat , 1991, The Journal of comparative neurology.

[13]  D. Crowne,et al.  Parietal and frontal eye field neglect in the rat , 1986, Behavioural Brain Research.

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

[15]  P. Goldman-Rakic,et al.  Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  L. Brown,et al.  Organizing principles of cortical integration in the rat neostriatum: Corticostriate map of the body surface is an ordered lattice of curved laminae and radial points , 1998, The Journal of comparative neurology.

[17]  D. Crowne,et al.  Some attentional effects of unilateral frontal lesions in the rat , 1982, Behavioural Brain Research.

[18]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[19]  A. Graybiel,et al.  Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body-part representations. , 1991, Journal of neurophysiology.

[20]  R. Roth,et al.  Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract‐tracing study with Phaseolus vulgaris leucoagglutinin , 1989, The Journal of comparative neurology.

[21]  J. Hoover,et al.  Overlapping corticostriatal projections from the rodent vibrissal representations in primary and secondary somatosensory cortex. , 2000, The Journal of comparative neurology.

[22]  H. Groenewegen,et al.  Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat , 1992, The Journal of comparative neurology.

[23]  R. Reep,et al.  Production and characterization of neglect in rats with unilateral lesions of ventrolateral orbital cortex , 1989, Experimental Neurology.

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

[25]  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.

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

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

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

[29]  Charles J. Wilson,et al.  Corticostriatal combinatorics: the implications of corticostriatal axonal arborizations. , 2002, Journal of neurophysiology.

[30]  A M Graybiel,et al.  The basal ganglia and adaptive motor control. , 1994, Science.

[31]  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.

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

[33]  J. Hoover,et al.  Divergent corticostriatal projections from a single cortical column in the somatosensory cortex of rats , 1998, Brain Research.

[34]  H. Künzle,et al.  Projections from the primary somatosensory cortex to basal ganglia and thalamus in the monkey , 1977, Experimental Brain Research.

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

[36]  R. Reep,et al.  Hemispheric asymmetry in neglect produced by unilateral lesions of dorsomedial prefrontal cortex in rats , 1988, Experimental Neurology.

[37]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

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

[39]  J. Donoghue,et al.  Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat , 1986, Brain Research.

[40]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[41]  M. Deschenes,et al.  Corticostriatal projections from layer V cells in rat are collaterals of long-range corticofugal axons , 1996, Brain Research.

[42]  K. Alloway,et al.  Organization of corticostriatal projections from the vibrissal representations in the primary motor and somatosensory cortical areas of rodents , 2001, The Journal of comparative neurology.

[43]  H. Künzle An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in macaca fascicularis. , 1978, Brain, behavior and evolution.

[44]  R. M. Beckstead An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal‐projection (prefrontal) cortex in the rat , 1979, The Journal of comparative neurology.

[45]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

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

[47]  I. Divac,et al.  Projections from the visual areas to the neostriatum in rats. A re-examination. , 1995, Acta neurobiologiae experimentalis.

[48]  G Mann,et al.  ON THE THALAMUS * , 1905, British medical journal.

[49]  Garrett E. Alexander Basal ganglia , 1998 .

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

[51]  D. Crowne,et al.  Effects of unilateral parietal lesions on spatial localization in the rat. , 1992, Behavioral neuroscience.

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