Elsevier

Neuroscience

Volume 29, Issue 3, 1989, Pages 503-537
Neuroscience

The organization of the projection from the cerebral cortex to the striatum in the rat

https://doi.org/10.1016/0306-4522(89)90128-0Get rights and content

Abstract

The detailed organization of the corticostriate projection has been investigated in the brain of the rat using the technique of retrograde transport of horseradish peroxidase following the placement of small, iontophoretic injections of horseradish peroxidase conjugated to lectin throughout all major regions of the striatum (caudate-putamen, nucleus accumbens and olfactory tubercle).

The results demonstrate that all major regions of the cerebral cortex project to the striatum on both sides of the brain with an ipsilateral predominance. The cells of origin of both the ipsilateral and contralateral corticostriate projections lie mainly in lamina V (especially lamina Va) with very small numbers in lamina III of the neocortex and mesocortex, and in the deep laminae of the allocortex. The results show that each striatal locus receives inputs from several cortical regions, i.e. there is extensive overlap in the corticostriate projection, and that, in general terms, each cortical region projects onto a longitudinally oriented region of the striatum. In particular, the major subdivisions of the cerebral cortex—the neocortex, mesocortex and allocortex—project onto defined but partially overlapping regions of the striatum: the neocortex projects to the caudate-putamen; the mesocortex projects mainly to the medial and ventral regions of the caudate-putamen but also to the ventral striatum (nucleus accumens and olfactory tubercle); and the allocortex projects mainly to the ventral striatum but also to the medial and ventral parts of the caudate-putamen. Within each of these major projection systems there is a further organization, with the constituent parts of each major cortical region projecting to smaller longitudinal components of the major projection fields. Each neocortical area projects to a longitudinal region of the dorsal striatum (caudate-putamen): the sensory and motor areas project topographically onto the dorsolateral striatum such that the rostral sensorimotor cortex (head areas) projects to central and ventral regions and the more caudal sensorimotor cortex (limb areas) projects to dorsal regions of the dorsolateral striatum; the visual area projects to the dorsomedial striatum; and the auditory area projects to the medial striatum. Each mesocortical area projects to a longitudinal area of the striatum: the most posteromedial mesocortex (the retrosplenial area) projects to the dorsomedial striatum; more anterior and lateral parts of the mesocortex project to more ventral parts of the striatum: and the most lateral mesocortex (the agranular insular and perirhinal areas) project to the ventrolateral striatum. The allocortical regions project to longutidinal regions of the ventral striatum: the entorhinal cortex projects throughout the ventral striatum and to the ventromedial caudate-putamen; the piriform cortex and archicortex (subiculum and hippocampus) project to partially overlapping regions of the ventral striatum and the medial caudate-putamen.

These findings provide the first detailed account of the overall organization of the corticostriate projection in the rat brain. The findings confirm and extend the concept of an extended striatial complex comprising the caudate-putamen, nucleus accumbens and olfactory tubercle which can be subdivided into two overlapping compartments on the basis of the pattern of cortical afferent connections: a large ventromedial limbic compartment related to the mesocortex and allocortex; and a smaller dorsolateral “non-limbic” compartment related to the neocortex. It is suggested that since all major regions of the cerebral cortex project in a bilateral fashion onto the striatum, the corticostriate projection may provide for the interhemispheric co-ordination of basal ganglia activity in the mammalian brain.

Reference (122)

  • FisherR.S. et al.

    Interhemispheric organization of corticocaudate projections in the cat: a retrograde double-labelling study

    Neurosci. Lett.

    (1984)
  • Garcia-RillE. et al.

    Projections to the neostriatum from the cat precruciate cortex. Anatomy and physiology

    Brain Res.

    (1979)
  • GerfenC.R. et al.

    An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin,Phaseolus vulgaris leucoagglutinin (PHA-L)

    Brain Res.

    (1984)
  • GraybielA.M. et al.

    A microelectrophoretic delivery technique for use with horseradish peroxidase

    Brain Res.

    (1974)
  • GraybielA.M. et al.

    Fiber connections of the basal ganglia

    Prog. Brain Res.

    (1979)
  • GroenewegenH.J. et al.

    Organization of the projections from the subiculum to the ventral striatum in the rat: a study using anterograde transport ofPhaseolus vulgaris leucoagglutinin

    Neuroscience

    (1987)
  • HedreenJ.C.

    Corticostriatal cells identified by the peroxidase method

    Neurosci. Lett.

    (1977)
  • JohnsonT.N. et al.

    Projections from behaviourally-defined sectors of the prefrontal cortex to the basal ganglia, septum and diencephalon of the monkey

    Expl Neurol.

    (1968)
  • KelleyA.E. et al.

    The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde and retrograde horseradish peroxidase study

    Neuroscience

    (1982)
  • KelleyA.E. et al.

    The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods

    Neuroscience

    (1982)
  • KitaiS.T. et al.

    Origin and characteristics of the cortico-caudate afferents: an anatomical and electrophysiological study

    Brain Res.

    (1976)
  • KrayniakP.F. et al.

    A projection from the entorhinal cortex to the nucleus accumbens in the rat

    Brain Res.

    (1981)
  • KunzleH.

    Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study inMacaca fascicularis

    Brain Res.

    (1975)
  • LeonardC.M.

    The prefrontal cortex in the rat.I. Cortical projections of the mediodorsal nucleus. II. Efferent connections

    Brain Res.

    (1969)
  • McGeorgeA.J. et al.

    The organization and collateralization of corticostriate neurones in the motor and sensory cortex of the rat brain

    Brain Res.

    (1987)
  • NeafseyE.J. et al.

    A second forelimb motor area exists in rat frontal cortex

    Brain Res.

    (1982)
  • PetrasJ.M.

    Connections of the parietal lobe

    J. Psychiat. Res.

    (1971)
  • PhillipsonO.T. et al.

    topographic order of inputs to nucleus accumbens in the rat

    Neuroscience

    (1985)
  • RagsdaleC.W. et al.

    The fronto-striatal projection in the cat and monkey and its relationship to inhomogeneities established by acetylcholinesterase histo-chemistry

    Brain Res.

    (1981)
  • ReepR.L. et al.

    Efferent connections of dorsal and ventral agranular insular cortex in the hamsterMesocricetus auratus

    Neuroscience

    (1982)
  • RoyceG.J.

    Cells of origin of subcortical afferents to the caudate nucleus: a horseradish peroxidase study in the cat

    Brain Res.

    (1978)
  • SandersonK.J. et al.

    Reevaluation of motor cortex and of sensorimotor overlap in cerebral cortex of albino rats

    Brain Res.

    (1984)
  • SchwabM. et al.

    Retrograde azonal transport of125I-tetanus toxin as a tool for tracing fiber connections in the central nervous system: connections of the rostral part of the rat neostriatum

    Brain Res.

    (1977)
  • SiegelA. et al.

    Projections of the hippocampus to the septal area in the squirrel monkey

    Brain Res.

    (1975)
  • SorensenK.E. et al.

    Entorhinal efferents reach the caudato-putamen

    Neurosci. Lett.

    (1983)
  • SwansonL.W. et al.

    A note on the connections and development of the nucleus accumbens

    Brain Res.

    (1975)
  • TanakaD.

    Corticostriate projections from reciprocally connected sectors of areas 4 and 5 in the dog

    Expl Neurol.

    (1983)
  • TanakaD. et al.

    Differential projections to the neostriatum from the arm areas of the primary and supplementary motor cortices in the dog

    Brain Res.

    (1979)
  • BaleydierC. et al.

    The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis

    Brain

    (1980)
  • BattagliniP.P. et al.

    Bilateral projections from the visual cortex to the striatum in the cat

    Expl Brain Res.

    (1982)
  • BecksteadR.M.

    An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal projection (prefrontal) cortex in the rat

    J. comp. Neurol.

    (1979)
  • BroadwellR.D.

    Olfactory relationships of the telencephalon and diencephalon in the rabbit. II. An autoradiographic and horseradish peroxidase study of the efferent connections of the anterior olfactory nucleus

    J. comp. Neurol.

    (1975)
  • CarmanJ.B. et al.

    The organisation of cortico-striate connections in the rabbit

    Brain

    (1963)
  • CarmanJ.B. et al.

    A bilateral cortico-straite projection

    J. Neurol.Neurosurg. Psychiat.

    (1965)
  • ChaplinJ.K. et al.

    Mapping of body representation in SI cortex of anaesthetized and awake rats

    J. comp. Neurol.

    (1984)
  • DafnyN. et al.

    A direct input from amygdaloid complex to caudate nucleus of the rat

    Expl Brain Res.

    (1975)
  • De OlmosJ.S.

    The amygdaloid projection field in the rat as studied with the cupric-silver method

  • De OlmosJ.S. et al.

    The projection field of the stria terminalis in the rat brain. An experimental study

    J. comp. Neurol.

    (1972)
  • De VitoJ.L. et al.

    Subcortical projections of the prefrontal lobe of the monkey

    J. comp. Neurol.

    (1964)
  • DonoghueJ.P. et al.

    A collateral pathway to the neostriatum from corticofugal neurons in the rat sensory motor cortex: an intracellular HRP study

    J. comp. Neurol.

    (1981)
  • Cited by (0)

    View full text