Cholecystokinin corticostriatal pathway in the rat: Evidence for bilateral origin from medial prefrontal cortical areas

doi:10.1016/0306-4522(94)90297-6

Neuroscience

Volume 59, Issue 4, April 1994, Pages 939-952

https://doi.org/10.1016/0306-4522(94)90297-6 Get rights and content

Abstract

The anterograde tracer Phaseolus vulgaris-leucoagglutinin was used to examine the organization of the projections to the striatum from medial prefrontal and frontal cortical areas in the rat with reference to their relation to cholecystokinin-like immunoreactivity in the striatum.

Medial prefrontal cortical areas projected bilaterally, with an ipsilateral predominance, to the striatum. Most of the positive fibres were found in medial and ventral areas of the caudate-putamen and in the nucleus accumbens. Labelled fibres formed distinct patch-like arrangements throughout the dorsomedial striatum, whereas more ventrally the fibres were densely packed and spread to lateral areas. Almost no fibres were found in the dorsolateral aspects of the caudate-putamen. Cholecystokinin-like immuno-reactivity in the striatum was diffusely distributed in the medial aspects, in fine punctate elements as well as in patches of fibres. Overlapping of corticostriatal clusters of fibres, from medial prefrontal cortex, with cholecystokinin-immunoreactive patches was found at all rostrocaudal levels studied, but predominantly in rostral areas. The overlap was present both in the ipsilateral and the contralateral side. Often the cluster of corticostriatal fibres was completely and precisely overlaid by a cholecystokinin-immunoreactive patch. At more caudal planes the overlap was only partial and in some instances cholecystokinin-positive patches “avoided” zones of dense corticostriatal fibre terminations.

Frontal cortex injections of tracer gave rise to a network of fibres in the lateral aspects of the striatum, sparing the medial areas. No overlap with cholecystokinin-immunoreactive patches was found in these cases.

These results suggest that a large number of cholecystokinin-containing striatal fibres originate in medial prefrontal cortical areas.

References (54)

BeinfeldM.C. et al.
The distribution of cholecystokinin immunoreactivity in the central nervous system of the rat as determined by radioimmunoassay
Brain Res.
(1981)
CarlssonM. et al.
Interactions between glutamatergic and monoaminergic systems within the basal ganglia—implications for schizophrenia and Parkinson's disease
Trends Neurosci.
(1990)
ClifferK.D. et al.
PHA-L can be transported anterogradely through fibers of passage
Brain Res.
(1988)
DalsassM. et al.
Medial prefrontal cortical projections to the region of the dorsal periventricular catecholamine system
Neuroscience
(1981)
DockrayG.J.
Cholecystokinins in rat cerebral cortex: identification, purification and characterization by immunochemical methods
Brain Res.
(1980)
DonoghueJ.P. et al.
Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat
Brain Res.
(1986)
FaggG.E. et al.
Amino acid neurotransmitters and their pathways in the mammalian central nervous system
Neuroscience
(1983)
FonnumF. et al.
Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibres in rat brain
Neuroscience
(1981)
FreyP.
Cholecystokinin octapeptide (CCK 26–33), nonsulfated octapeptide and tetrapeptide (CCK 30–33) in rat brain: analysis by high pressure liquid chromatography (HPLC) and raadioimmunoassay (RIA)
Neurochem. Int.
(1983)
GerfenC.R. et al.
An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axon and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L)
Brain Res.
(1984)

GraybielA.M. et al.

An immunohistochemical study of enkephalins and other neuropeptides in the striatum of the cat with evidence that the opiate peptides are arranged to form mosaic patterns in register with the striosomal compartments visible by acetylcholinesterase staining

Neuroscience

(1981)

GraybielA.M. et al.

Fiber connections of the basal ganglia

Prog. Brain Res.

(1979)

HökfeltT. et al.

A subpopulation of mesencephalic dopamine neurons projecting to limbic areas contains a cholecystokinin-like peptide: evidence from immunohistochemistry combined with retrograde tracing

Neuroscience

(1980)

KimJ.-S. et al.

Effect of frontal cortex ablation on striatal glutamic acid level in rat

Brain Res.

(1977)

KrayniakP.F. et al.

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

Brain Res.

(1981)

McGeerP.L. et al.

A glutamatergic corticostriatal pathway

Brain Res.

(1977)

MeyerD.K. et al.

Bilateral ablation of frontal cortex reduces concentration of cholecystokinin-like immunoreactivity in rat dorsolateral striatum

Brain Res.

(1988)

MorinoP. et al.

Immunohistochemical evidence for a crossed cholecystokinin corticostriatal pathway in the rat

Neurosci. Lett.

(1992)

ReubiJ.C. et al.

Glutamate releasein vitro from corticostriatal terminals

Brain Res.

(1979)

SchofieldB.R.

Uptake of Phaseolus vulgaris leucoagglutinin (PHA-L) by axons of passage

J. Neurosci. Meth.

(1990)

SörensenK.E. et al.

Entorhinal efferents reach the caudato-putamen

Neurosci. Lett.

(1983)

VeeningJ.G. et al.

The topical organization of the afferents to the caudato-putamen of the rat. A horseradish peroxidase study

Neuroscience

(1980)

ZaborszkyL. et al.

Cholecystokinin innervation of the ventral striatum: morphological and radioimmunological study

Neuroscience

(1985)

BecksteadR.M.

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

J. comp. Neurol.

(1979)

BerendseH.W. et al.

Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat

J. comp. Neurol.

(1992)

BurgunderJ.-M. et al.

Cortical neurons expressing the cholecystokinin gene in the rat: distribution in the adult brain, ontogeny, and some of their projections

J. comp. Neurol.

(1990)

FonnumF. et al.

Identification of excitatory amino acid pathways in the mammalian nervous system

Cited by (35)

Influences of social reward experience on behavioral responses to drugs of abuse: Review of shared and divergent neural plasticity mechanisms for sexual reward and drugs of abuse
2017, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
For reviews on D1 and D2 receptor functions, see (Hikida et al., 2016; Soares-Cunha et al., 2016). Along with dopamine input, the NAc also receives glutamatergic projections from the subiculum and amygdala (Phillipson and Griffiths, 1985), hippocampus (Zaczek et al., 1979), thalamus (Phillipson and Griffiths, 1985) and prefrontal cortex (Phillipson and Griffiths, 1985; Buchanan et al., 1994; Morino et al., 1994; Montaron et al., 1996; Gorelova and Yang, 1997; Ferry et al., 2000; Chiba et al., 2001), and these afferents form asymmetric synapses on the same MSNs that receive dopamine inputs (Sesack et al., 2003) to convey reward information during goal-directed behavior (Papp et al., 2012). For instance, optogenetic inhibition of glutamatergic inputs from the BLA- or ventral hippocampus- to the NAc reduced cue-induced sucrose intake (Stuber et al., 2011) or inhibited cocaine-induced locomotion (Britt et al., 2012), respectively.
Different factors influence the development of drug addiction in humans, including social reward experiences. In animals, experience with social rewards, such as sexual behavior, pair bonding, social and environmental enrichment, can be protective. However, loss or lack of social rewards can lead to a vulnerability to drug-seeking behavior. The effects of social reward experience on drug-seeking behavior are associated with changes in the neural pathways that control drug-related behavior. This review will provide an introduction and overview of the mesolimbic pathway and the influence of social reward experience on drug-seeking behavior in rodents. Moreover, the research from our laboratory on effects of sexual experience and loss of sex reward on psychostimulant and opiate reward will be reviewed. Finally, we will review current knowledge of the neural mechanisms that underlie these interactions. Investigations of the neural underpinnings by which social and drug rewards interact contribute to improved understanding of the neural basis of vulnerability for drug addiction and reward-related behaviors in general.
Cholecystokinin is necessary for the expression of morphine conditioned place preference
2006, Pharmacology Biochemistry and Behavior
There is evidence that the neuropeptide cholecystokinin (CCK) is important for the rewarding effects of drugs of abuse. However, less is known regarding the role of CCK in drug seeking and craving. The present study investigated whether the CCK_B antagonist L-365, 260 could block morphine-induced drug seeking using the conditioned place preference paradigm and whether the dopaminergic reward pathway contributes to the effect of L-365, 260 on expression of morphine place preference. We found that systemic administration of the CCK_B antagonist L-365, 260 attenuates the expression of morphine-induced drug seeking as assessed using conditioned place preference (CPP) and shows that this effect is mediated by CCK_B receptors in the anterior nucleus accumbens (NAcc). Additionally, we demonstrate that this effect is dependent on D₂ receptor activation in the anterior nucleus accumbens (NAcc). These results indicate that endogenous CCK modulates the incentive-salience of morphine-associated cues and suggest that CCK antagonists may be useful in the treatment of drug craving.
Overlapping regional distribution of CCK and TPPII mRNAs in Cynomolgus monkey brain and correlated levels in human cerebral cortex (BA 10)
2006, Brain Research
Citation Excerpt :
Gene expression for CCK shows a similar distribution as the peptide and CCK B receptor except for regions such as the caudate-putamen and cerebellum, where scarce or no detectable levels of CCK mRNA can be found (Lindefors et al., 1991; Lindefors et al., 1993; Schiffmann and Vanderhaeghen, 1991). The CCK-like immunoreactive material detected in the caudate-putamen originates from projecting neurons located elsewhere (cortical regions and mesolimbic neurons) (Burgunder and Young, 1990; Hokfelt et al., 1980; Morino et al., 1994b). CCK-8 is the main form of CCK in mammalian brain (Dockray, 1980), but both larger and smaller biologically active C-terminal fragments such as CCK-58, CCK-33 CCK-5 and CCK-4 are also detectable in different species including human (Larsson and Rehfeld, 1979; Lindefors et al., 1993).
Tripeptidyl peptidase II (TPPII) is a high molecular weight exopeptidase important in inactivating extracellular cholecystokinin (CCK). Our aims were to study the anatomical localization of TPPII and CCK mRNA in the Cynomolgus monkey brain as a basis for a possible functional anatomical connection between enzyme (TPPII) and substrate (CCK) and examine if indications of changes in substrate availability in the human brain might be reflected in changes of levels of TPPII mRNA. Methods: mRNA in situ hybridization on postmortem brain from patients having had a schizophrenia diagnosis as compared to controls and on monkey and rat brain slices. Results: overlapping distribution patterns of mRNAs for TPPII and CCK in rat and monkey. High amounts of TPPII mRNA are seen in the neocortex, especially in the frontal region and the hippocampus. TPPII mRNA is also present in the basal ganglia and cerebellum where CCK immunoreactivity and/or CCK B receptors have been found in earlier studies, suggesting presence of CCK-ergic afferents from other brain regions. Levels of mRNAs for CCK and TPPII show a positive correlation in postmortem human cerebral cortex Brodmann area (BA) 10. TPPII mRNA might be affected following schizophrenia. Discussion: overall TPPII and CCK mRNA show a similar distribution in rat and monkey brain, confirming and extending earlier studies in rodents. In addition, correlated levels of TPPII and CCK mRNA in human BA 10 corroborate a functional link between CCK and TPPII in the human brain.
What we know and what we need to know about the role of endogenous CCK in psychostimulant sensitization
2003, Life Sciences
Citation Excerpt :
Some of the remaining CCK in the core comes from the cerebral cortex (Meyer et al., 1982; Zaborsky et al., 1985). CCK is co-localized with glutamate in the prefrontal cortex(Morino et al., 1992, 1994a,b) and it is these CCK neurons that provide the bulk of the CCK to the dorsal striatum. Cerebral cortical CCK neurons have been shown to release CCK in the nucleus accumbens.
The unique distribution of CCK and its receptors and its co-localization with dopamine makes it ideally situated to pay a role in dopamine-mediated reward and psychostimulant sensitization. A number of studies support the hypothesis that CCK acting through the CCK 1 and CCK 2 receptors is an endogenous modulator of dopamine neurotransmission. Behavioral studies with CCK antagonists and CCK 1 receptor mutant rats support a role for endogenous CCK in behavioral sensitization to psychostimulants. CCK microdialysis studies in the nucleus accumbens (NAC) have demonstrated that extracellular CCK is increased in the NAC by psychostimulants, providing neurochemical evidence that CCK could be involved in the behavioral response to psychostimulants. A model for how CCK may be acting in multiple brain regions to foster sensitization is presented and the gaps in our knowledge about the role of CCK in psychostimulant sensitization are described.
Comparative analysis of the central CCK system in Fawn Hooded and Wistar Kyoto rats: Extended localisation of CCK-A receptors throughout the rat brain using a novel radioligand
2001, Regulatory Peptides
The neuropeptide cholecystokinin has been implicated in the actions of a number of central processes including anxiety and reward. For this reason, the aim of the present study was to compare the density of CCK-A and -B receptors and the mRNA encoding preproCCK throughout the brains of an alcohol-preferring (Fawn Hooded) rat strain with that of a non-alcohol-preferring (Wistar Kyoto) strain of rat. Our study revealed significant differences with regard to the central CCK system of the FH compared to the WKY rat, including differences in CCK-A receptor binding throughout the dorsal medulla, and altered CCK-B binding density throughout the cerebral cortex and reticular nucleus of the thalamus. The most striking result, given the altered behavioural phenotype of the FH rat, was the 33% lower density of CCKmRNA measured throughout the ventral tegmental area of the FH rat when compared to the WKY. This study also reports on a protocol to utilise a novel radioligand, [¹²⁵I]-d-Tyr-Gly-A-71378, for autoradiographic detection of CCK-A receptors throughout the rat brain. As previously reported, CCK-A receptors were located throughout the area postrema, interpeduncular nucleus and nucleus tractus solitarii; however, binding to CCK-A receptors was also visualised throughout the medial pre-optic area, the arcuate nucleus and the circumventricular regions of the ventral hypothalamus, regions known to contain CCK-A receptors but which were previously undetectable using autoradiography in rat brain.
Interactive effects of cholecystokinin-8S and various serotonin receptor agonists on the firing activity of neostriatal neurones in rats
2001, Neuropeptides
In rats anaesthetized with urethane single unit activity was extracellularly recorded in the neostriatum, and several drugs were microiontophoretically ejected. Separate administration of the sulfated octapeptide cholecystokinin (CCK-8S), serotonin (5-HT) or 8-OH-DPAT (a 5-HT_1A/7 receptor agonist) predominantly induced increases in the neuronal discharge rates (Wilcoxon test significant P<0.05), whereas the 5-HT_2A/2C receptor agonist DOI affected only a few neurones and mainly reduced firing. After coadministration of CCK-8S and serotonin, activating effects alsopredominated (Wt P<0.05), but the neuronal responsiveness was significantly reduced (Chi²P<0.01). Similarly, concomitant application of CCK-8S and 8-OH-DPAT led to significant activation accompanied with a reduction of inhibitory effects. The block of serotonin- or 8-OH-DPAT-effects through specific 5-HT_1A receptor antagonists impliesthe involvement of this receptor subtype within the striatum. In conclusion, concomitant action of CCK-8S and serotonin induces a mean level of neuronal activation that might promote normal function.

View all citing articles on Scopus

View full text

Cholecystokinin corticostriatal pathway in the rat: Evidence for bilateral origin from medial prefrontal cortical areas

Abstract

Brain Res.

Trends Neurosci.

Brain Res.

Neuroscience

Brain Res.

Brain Res.

Neuroscience

Neuroscience

Neurochem. Int.

Brain Res.

Neuroscience

Prog. Brain Res.

Neuroscience

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Neurosci. Lett.

Brain Res.

J. Neurosci. Meth.

Neurosci. Lett.

Neuroscience

Neuroscience

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

J. comp. Neurol.

Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat

J. comp. Neurol.

Cortical neurons expressing the cholecystokinin gene in the rat: distribution in the adult brain, ontogeny, and some of their projections

J. comp. Neurol.

Identification of excitatory amino acid pathways in the mammalian nervous system