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brain sciences Review Parallel Emergence of a Compartmentalized Striatum with the Phylogenetic Development of the Cerebral Cortex Tadashi Hamasaki 1 and Satoshi Goto 2,3,* 1 Department of Neurosurgery, Kumamoto University Medical School, Kumamoto 860-8556, Japan; [email protected] 2 Department of Neurodegenerative Disorders Research, Institute of Biomedical Sciences, Graduate School of Medical Sciences, Tokushima University, Tokushima 770-8503, Japan 3 Parkinson’s Disease and Dystonia Research Center, Tokushima University Hospital, Tokushima University, Tokushima 770-8503, Japan * Correspondence: [email protected]; Tel.: +81-88-633-7206; Fax: +81-88-633-7208 Received: 7 March 2019; Accepted: 17 April 2019; Published: 19 April 2019 Abstract: The intricate neuronal architecture of the striatum plays a pivotal role in the functioning of the basal ganglia circuits involved in the control of various aspects of motor, cognitive, and emotional functions. Unlike the cerebral cortex, which has a laminar structure, the striatum is primarily composed of two functional subdivisions (i.e., the striosome and matrix compartments) arranged in a mosaic fashion. This review addresses whether striatal compartmentalization is present in non-mammalian vertebrates, in which simple cognitive and behavioral functions are executed by primitive sensori-motor systems. Studies show that neuronal subpopulations that share neurochemical and connective properties with striosomal and matrix neurons are present in the striata of not only anamniotes (fishes and amphibians), but also amniotes (reptiles and birds). However, these neurons do not form clearly segregated compartments in these vertebrates, suggesting that such compartmentalization is unique to mammals. In the ontogeny of the mammalian forebrain, the later-born matrix neurons disperse the early-born striosome neurons into clusters to form the compartments in tandem with the development of striatal afferents from the cortex. We propose that striatal compartmentalization in mammals emerged in parallel with the evolution of the cortex and possibly enhanced complex processing of sensory information and behavioral flexibility phylogenetically. Keywords: compartmentalization; matrix; striosome; phylogenetic development: striatum; vertebrate 1. Introduction The striatum is a key component of the basal ganglia circuit, which is involved in normal motor, cognitive, and emotional functions. Dysregulation of striatal function contributes to a variety of neurological and neurobehavioral disorders [1]. Accurate processing in the basal ganglia circuit is thus required for normal movements and behaviors in humans and depends on a balance between input and output neurotransmission, which in turn is reinforced by an organized cellular architecture [1]. The striatum is the primary receptive nucleus of the basal ganglia circuit and receives inputs from all cortical areas. However, the structural organization of the mammalian striatum is unique and is characterized by a mosaic pattern, distinct from the laminar cerebral cortex [2,3]. Two neurochemically-specified subdivisions, i.e., striosomes (patches) and the extrastriosomal matrix, exist in the mammalian striatum. This novel arrangement is related to neurotransmitter interactions and striatal input and output systems. The striosome is organized in a labyrinthine structure in 3D Brain Sci. 2019, 9, 90; doi:10.3390/brainsci9040090 www.mdpi.com/journal/brainsci Brain Sci. 2019, 9, x FOR PEER REVIEW 2 of 14 Brain Sci. 2019, 9, 90 2 of 14 exist in the mammalian striatum. This novel arrangement is related to neurotransmitter interactions and striatal input and output systems. The striosome is organized in a labyrinthine structure in 3D space,space, andand the the matrix matrix occupies occupies the spacethe space surrounding surroun theding striosome. the striosome. The matrix-based The matrix-based output pathway output actspathway as a push-pullacts as a push-pull system to increasesystem to or increase decrease or movement decrease movement through direct through or indirect direct or pathways, indirect respectivelypathways, respectively [1]. The striosomal [1]. The striosomal pathway pathway likely exerts likely critical exerts motor critical control motor control by modulating by modulating nigral dopaminergicnigral dopaminergic outputs [outputs2,4]. Growing [2,4]. evidenceGrowing suggestsevidence that suggests the dysregulation that the dysregulation of striatal compartments of striatal mightcompartments cause movement might cause disorders movement [1,5–7 disorders]. [1,5–7]. LittleLittle isis known known about about striatal striatal compartmentalization compartmentalization in non-mammalian in non-mammalian vertebrates vertebrates with primitive with motorprimitive functions motor andfunctions behaviors. and Inbehaviors. this review, In wethis focusreview, on whetherwe focus the on mosaic whether organization the mosaic of theorganization striatum isof uniquethe striatum to animals is unique with to animals well-developed with well-developed cerebral cortices. cerebral We cortices. postulate We thatpostulate clear compartmentalizationthat clear compartmentalization in the striatum in the striatum emerges em parallelerges parallel to the to phylogenetic the phylogenetic development development of the of cerebralthe cerebral cortex. cortex. Do neurochemically-identified Do neurochemically-identifi striosomeed striosome and matrix and neurons matrix exist neurons in non-mammalian exist in non- vertebratesmammalian or vertebrates anamniotes? or Neurochemicalanamniotes? Neurochemica markers to distinguishl markers striosometo distinguish and matrixstriosome compartments and matrix werecompartments extensively were reviewed extensively by Crittenden reviewed and by Graybiel Crittenden [1]. Forand example, Graybiel D1-type [1]. For dopamine example, receptorD1-type (D1R),dopamine glutamate receptor receptor, (D1R), ionotropic,glutamate receptor, AMPA 1 (GluR1),ionotropic, substance AMPA P1 (SP),(GluR1), and substance tyrosine hydroxylase P (SP), and (TH)tyrosine in dopaminergichydroxylase (TH) afferent in terminalsdopaminergic were affe markersrent terminals for the striosome. were markers Acetylcholine for the striosome. esterase (AChE),Acetylcholine calbindin esterase (CB), (AChE), choline calbindin acetyltransferase (CB), cho (ChAT),line acetyltransferase enkephalin (ENK), (ChAT), and enkephalin neuropeptide (ENK), Y (NPY)and neuropeptide were markers Y (NPY) for the were matrix. markers Here, for we the review matrix. the Here, literature we review on expression the literature patterns on expression of striatal compartmentpatterns of striatal markers compartment throughout markers the vertebrate throughout phylogeny the vertebrate (for reference phylogeny see, Figure (for1). reference Evolutional see, changesFigure 1). in fundamentalEvolutional architectureschanges in fundamental in the striatum architectures were extensively in the addressed striatum bywere Reiner extensively et al. [8] andaddressed Smeets by et Reiner al. [9] and et al. are [8] not and presented Smeets et in al. this [9] review. and are not presented in this review. FigureFigure 1.1. AA phylogeneticphylogenetic treetree ofof vertebratevertebrate evolution.evolution. AA diagramdiagram showingshowing thethe lineslines ofof evolutionaryevolutionary descentdescent ofof didifferentfferent vertebratesvertebrates fromfrom aa commoncommon ancestor.ancestor. TheThe ancestralancestral bonybony fishfish gavegave riserise toto ancestralancestral amphibians.amphibians. Through Through water-land water-land transition, ancest ancestralral amphibians gave rise to stem anamniotes,anamniotes, whichwhich thenthen separatelyseparately evolvedevolved intointo sauropsidssauropsids andand therapsids.therapsids. SauropsidsSauropsids areare notnot onlyonly thethe ancestorsancestors ofof existing reptiles but but also also gave gave rise rise to to the the ancestors ancestors of birds. of birds. Mammalian Mammalian species species have have evolved evolved from fromtherapsid therapsid ancestors, ancestors, although although many many groups groups of the of therapsids the therapsids have have become become extinct extinct (dashed (dashed line). line). The Thesix-layered six-layered cortex cortex waswas inherited inherited by the by mammalian the mammalian ancestor ancestor of therapsids of therapsids (green (green line) line) more more than than 200 200million million years years ago ago[10]. [10 Modified]. Modified from from Jarvis Jarvis et al. et [11]. al. [11 ]. 2. The Striatum in Anamniotes 2. The Striatum in Anamniotes Although the structure of the basal ganglia in early vertebrates has been extensively studied [12–15], Although the structure of the basal ganglia in early vertebrates has been extensively studied [12– little is known about striatal compartmentalization. Major neurotransmitters such as acetylcholine 15], little is known about striatal compartmentalization. Major neurotransmitters such as and dopamine, neuropeptides such as SP and ENK, and related enzyme systems such as AChE or acetylcholine and dopamine, neuropeptides such as SP and ENK, and related enzyme systems such TH, developed very early in animal evolution [8]. Their expression patterns can thus be used to study as AChE or TH, developed very early in animal evolution [8]. Their expression patterns can thus be structural differences of the basal ganglia in diverse living anamniote species. used to study structural differences of the