The orbital cortex in rats topographically projects to central parts of the caudate–putamen complex

Disturbances of the orbitofrontal-striatal pathways in humans have been associated with several psychopathologies including obsessive-compulsive disorder and drug addiction. In nonhuman primates, different subareas of the orbitofrontal cortex project topographically to central and ventromedial parts of the striatum. Relatively little is known about the anatomical organization of the rat orbital cortex while there is a growing interest in this cortical area from a functional and behavioral point of view. The aim of the present neuroanatomical tracing study was to determine in rats the striatal target area of the projections of the orbital cortex as well as the topographical organization within these projections. To this end, anterograde tracers were injected in the different cytoarchitectonically distinct subareas of the orbital cortex. The results show that the individual orbital areas, i.e. medial orbital area, ventral orbital area, ventrolateral orbital area and lateral orbital area, project to central parts of the caudate-putamen, exhibiting a mediolateral and, to a lesser degree, rostrocaudal topographical arrangement. Orbital projections avoid the most dorsal, as well as rostral and caudal parts of the caudate-putamen. Terminal fields from cytoarchitectonically different areas show a considerable overlap. Superficial cortical layers project preferentially to the striatal matrix, deep layers to the patch compartment. The projections from the ventrolateral orbital area are strongest and occupy the most extensive striatal area. In addition to projections to the caudate-putamen, the ventrolateral, lateral and dorsolateral orbital areas have a scarce projection to the most lateral part of the nucleus accumbens shell in the ventral striatum. In contrast to nonhuman primates, the remainder of the rat nucleus accumbens is virtually free of orbital projections.

[1]  C. Pennartz,et al.  Anatomical evidence for direct connections between the shell and core subregions of the rat nucleus accumbens , 2005, Neuroscience.

[2]  H. Steinbusch,et al.  Distribution of serotonin-immunoreactivity in the central nervous system of the rat—Cell bodies and terminals , 1981, Neuroscience.

[3]  J. Feldon,et al.  Effect of excitotoxic lesions of rat medial prefrontal cortex on spatial memory , 2002, Behavioural Brain Research.

[4]  B. Kolb,et al.  Do rats have a prefrontal cortex? , 2003, Behavioural Brain Research.

[5]  C. Saper,et al.  Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat , 1987, The Journal of comparative neurology.

[6]  C. Gerfen,et al.  The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  J. Price,et al.  The organization of the thalamocortical connections of the mediodorsal thalamic nucleus in the rat, related to the ventral forebrain–prefrontal cortex topography , 1992, The Journal of comparative neurology.

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

[9]  H. Uylings,et al.  Reduced orbitofrontal-striatal activity on a reversal learning task in obsessive-compulsive disorder. , 2006, Archives of general psychiatry.

[10]  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.

[11]  J. Price,et al.  Prefrontal cortical projections to the striatum in macaque monkeys: Evidence for an organization related to prefrontal networks , 2000, The Journal of comparative neurology.

[12]  J. Pujol,et al.  Mapping structural brain alterations in obsessive-compulsive disorder. , 2004, Archives of general psychiatry.

[13]  N. Volkow,et al.  The neural basis of addiction: a pathology of motivation and choice. , 2005, The American journal of psychiatry.

[14]  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.

[15]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[16]  V. Bagaev,et al.  Visceral-related area in the rat insular cortex , 2006, Autonomic Neuroscience.

[17]  C. Cavada,et al.  The anatomical connections of the macaque monkey orbitofrontal cortex. A review. , 2000, Cerebral cortex.

[18]  Harry B. M. Uylings,et al.  The rat orbital and agranular insular prefrontal cortical areas: a cytoarchitectonic and chemoarchitectonic study , 2008, Brain Structure and Function.

[19]  N. Volkow,et al.  Cocaine Cues and Dopamine in Dorsal Striatum: Mechanism of Craving in Cocaine Addiction , 2006, The Journal of Neuroscience.

[20]  T. Robbins,et al.  Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates , 2004, Neuroscience & Biobehavioral Reviews.

[21]  J. R. Baker,et al.  Functional magnetic resonance imaging of symptom provocation in obsessive-compulsive disorder. , 1996, Archives of general psychiatry.

[22]  P. Blier,et al.  Mechanisms of action of current and potential pharmacotherapies of obsessive-compulsive disorder , 2006, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

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

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

[25]  M. Kringelbach The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[26]  H. Groenewegen,et al.  The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics , 2003, Neuroscience & Biobehavioral Reviews.

[27]  S. Rauch,et al.  Functional neuroimaging and the neuroanatomy of obsessive-compulsive disorder. , 2000, The Psychiatric clinics of North America.

[28]  I. Törk Anatomy of the Serotonergic System a , 1990, Annals of the New York Academy of Sciences.

[29]  H. Groenewegen,et al.  Patterns of overlap and segregation between insular cortical, intermediodorsal thalamic and basal amygdaloid afferents in the nucleus accumbens of the rat , 1996, Neuroscience.

[30]  H. Groenewegen,et al.  Basal amygdaloid complex afferents to the rat nucleus accumbens are compartmentally organized , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  A. Roberts,et al.  Primate orbitofrontal cortex and adaptive behaviour , 2006, Trends in Cognitive Sciences.

[32]  Henk J Groenewegen,et al.  Frontal-striatal dysfunction during planning in obsessive-compulsive disorder. , 2005, Archives of general psychiatry.

[33]  J. Kulisevsky,et al.  Obsessive-compulsive disorder associated with brain lesions , 1996, Neurology.

[34]  D. Joel,et al.  Role of the orbital cortex and of the serotonergic system in a rat model of obsessive compulsive disorder , 2005, Neuroscience.

[35]  T. Robbins,et al.  Dissociable Forms of Inhibitory Control within Prefrontal Cortex with an Analog of the Wisconsin Card Sort Test: Restriction to Novel Situations and Independence from “On-Line” Processing , 1997, The Journal of Neuroscience.

[36]  E. Lynd-Balta,et al.  The orbital and medial prefrontal circuit through the primate basal ganglia , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  G. Schoenbaum,et al.  Integrating orbitofrontal cortex into prefrontal theory: common processing themes across species and subdivisions. , 2001, Learning & memory.

[38]  D. Joel,et al.  The effects of temporary inactivation of the orbital cortex in the signal attenuation rat model of obsessive compulsive disorder. , 2006, Behavioral neuroscience.

[39]  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.