Conservation of the Direct and Indirect Pathway Dichotomy in Mouse Caudal Striatum With Uneven Distribution of Dopamine Receptor D1- and D2-Expressing Neurons

The striatum is one of the key nuclei for adequate control of voluntary behaviors and reinforcement learning. Two striatal projection neuron types, expressing either dopamine receptor D1 (D1R) or dopamine receptor D2 (D2R) constitute two independent output routes: the direct or indirect pathways, respectively. These pathways co-work in balance to achieve coordinated behavior. Two projection neuron types are equivalently intermingled in most striatal space. However, recent studies revealed two atypical zones in the caudal striatum: the zone in which D1R-neurons are the minor population (D1R-poor zone) and that in which D2R-neurons are the minority (D2R-poor zone). It remains obscure as to whether these imbalanced zones have similar properties on axonal projections and electrophysiology compared to other striatal regions. Based on morphological experiments in mice using immunofluorescence, in situ hybridization, and neural tracing, here, we revealed that the poor zones densely projected to the globus pallidus and substantia nigra pars lateralis, with a few collaterals in substantia nigra pars reticulata and compacta. Similar to that in other striatal regions, D1R-neurons were the direct pathway neurons. We also showed membrane properties of projection neurons in the poor zones were largely similar to those in the conventional striatum using in vitro electrophysiological recording. In addition, the poor zones existed irrespective of the age or sex of mice. We also identified the poor zones in the common marmoset as well as other rodents. These results suggest that the poor zones in the caudal striatum follow the conventional projection patterns irrespective of imbalanced distribution of projection neurons. The poor zones could be an innate structure and common in mammals. The unique striatal zones possessing highly restricted projections could relate to functions different from those of motor-related striatum.

[1]  Shin Ishii,et al.  Cellular-resolution gene expression profiling in the neonatal marmoset brain reveals dynamic species- and region-specific differences , 2021, Proceedings of the National Academy of Sciences.

[2]  Li I. Zhang,et al.  Corticostriatal control of defense behavior in mice induced by auditory looming cues , 2021, Nature Communications.

[3]  E. Valjent,et al.  The Tail of the Striatum: From Anatomy to Connectivity and Function , 2020, Trends in Neurosciences.

[4]  Nicholas N. Foster,et al.  The mouse cortico–basal ganglia–thalamic network , 2020, Nature.

[5]  Hyoung F. Kim,et al.  Optogenetic manipulation of a value-coding pathway from the primate caudate tail facilitates saccadic gaze shift , 2020, Nature Communications.

[6]  A. Zador,et al.  Corticostriatal Plasticity Established by Initial Learning Persists after Behavioral Reversal , 2020, eNeuro.

[7]  Talia N. Lerner,et al.  Amygdala-Midbrain Connections Modulate Appetitive and Aversive Learning , 2020, Neuron.

[8]  T. Ellender,et al.  Dynamic postnatal development of the cellular and circuit properties of striatal D1 and D2 spiny projection neurons , 2019, The Journal of physiology.

[9]  A. Nishi,et al.  Three divisions of the mouse caudal striatum differ in the proportions of dopamine D1 and D2 receptor-expressing cells, distribution of dopaminergic axons, and composition of cholinergic and GABAergic interneurons , 2019, Brain Structure and Function.

[10]  O. Hikosaka,et al.  Indirect pathway from caudate tail mediates rejection of bad objects in periphery , 2019, Science Advances.

[11]  F. Fujiyama,et al.  Motor cortex can directly drive the globus pallidus neurons in a projection neuron type-dependent manner in the rat , 2019, bioRxiv.

[12]  E. Valjent,et al.  Contrasting patterns of ERK activation in the tail of the striatum in response to aversive and rewarding signals , 2019, bioRxiv.

[13]  A. Nishi,et al.  Striosome-based map of the mouse striatum that is conformable to both cortical afferent topography and uneven distributions of dopamine D1 and D2 receptor-expressing cells , 2018, Brain Structure and Function.

[14]  Brian S. Eastwood,et al.  Topographic precision in sensory and motor corticostriatal projections varies across cell type and cortical area , 2018, Nature Communications.

[15]  Karl Deisseroth,et al.  Mapping projections of molecularly defined dopamine neuron subtypes using intersectional genetic approaches , 2018, Nature Neuroscience.

[16]  N. Uchida,et al.  Dopamine neurons projecting to the posterior striatum reinforce avoidance of threatening stimuli , 2018, Nature Neuroscience.

[17]  B. Balleine,et al.  From learning to action: the integration of dorsal striatal input and output pathways in instrumental conditioning , 2018, The European journal of neuroscience.

[18]  D. Popa,et al.  Active intermixing of indirect and direct neurons builds the striatal mosaic , 2018, bioRxiv.

[19]  Hyoung F. Kim,et al.  Anatomical Inputs From the Sensory and Value Structures to the Tail of the Rat Striatum , 2018, Front. Neuroanat..

[20]  Ali Ghazizadeh,et al.  Flexible and Stable Value Coding Areas in Caudate Head and Tail Receive Anatomically Distinct Cortical and Subcortical Inputs , 2017, Front. Neuroanat..

[21]  H. Okano,et al.  Digital gene atlas of neonate common marmoset brain , 2017, Neuroscience Research.

[22]  V. Kotak,et al.  The Sensory Striatum Is Permanently Impaired by Transient Developmental Deprivation. , 2017, Cell reports.

[23]  Hyoung F. Kim,et al.  Indirect Pathway of Caudal Basal Ganglia for Rejection of Valueless Visual Objects , 2017, Neuron.

[24]  A. Parent,et al.  A dense cluster of D1+ cells in the mouse nucleus accumbens , 2017, Synapse.

[25]  N. Uchida,et al.  Opposite initialization to novel cues in dopamine signaling in ventral and posterior striatum in mice , 2016, eLife.

[26]  Tianyi Mao,et al.  A comprehensive excitatory input map of the striatum reveals novel functional organization , 2016, eLife.

[27]  S. Shipp The functional logic of corticostriatal connections , 2016, Brain Structure and Function.

[28]  Nicholas N. Foster,et al.  The mouse cortico-striatal projectome , 2016, Nature Neuroscience.

[29]  J. Blesa,et al.  Selective connectivity of dopamine neurons projecting to the posterior striatum , 2016, Movement disorders : official journal of the Movement Disorder Society.

[30]  Sachie K. Ogawa,et al.  Dopamine neurons projecting to the posterior striatum form an anatomically distinct subclass , 2015, eLife.

[31]  Hyoung F. Kim,et al.  Parallel basal ganglia circuits for voluntary and automatic behaviour to reach rewards. , 2015, Brain : a journal of neurology.

[32]  O. Hikosaka,et al.  Functional territories in primate substantia nigra pars reticulata separately signaling stable and flexible values. , 2015, Journal of neurophysiology.

[33]  Hyoung F. Kim,et al.  Separate groups of dopamine neurons innervate caudate head and tail encoding flexible and stable value memories , 2014, Front. Neuroanat..

[34]  A. Zador,et al.  Selective corticostriatal plasticity during acquisition of an auditory discrimination task , 2014, Nature.

[35]  P. Calabresi,et al.  Direct and indirect pathways of basal ganglia: a critical reappraisal , 2014, Nature Neuroscience.

[36]  Alexxai V. Kravitz,et al.  Working together: basal ganglia pathways in action selection , 2014, Trends in Neurosciences.

[37]  Hyoung F. Kim,et al.  Distinct Basal Ganglia Circuits Controlling Behaviors Guided by Flexible and Stable Values , 2013, Neuron.

[38]  J. Girault,et al.  Spatial distribution of D1R- and D2R-expressing medium-sized spiny neurons differs along the rostro-caudal axis of the mouse dorsal striatum , 2013, Front. Neural Circuits.

[39]  Y. Isomura,et al.  Reward-Modulated Motor Information in Identified Striatum Neurons , 2013, The Journal of Neuroscience.

[40]  G. Shepherd Corticostriatal connectivity and its role in disease , 2013, Nature Reviews Neuroscience.

[41]  Steven S. Vogel,et al.  Concurrent Activation of Striatal Direct and Indirect Pathways During Action Initiation , 2013, Nature.

[42]  C. Gerfen,et al.  Distribution and compartmental organization of GABAergic medium-sized spiny neurons in the mouse nucleus accumbens , 2012, Front. Neural Circuits.

[43]  Ilya E. Monosov,et al.  What and Where Information in the Caudate Tail Guides Saccades to Visual Objects , 2012, The Journal of Neuroscience.

[44]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[45]  Sachie K. Ogawa,et al.  Whole-Brain Mapping of Direct Inputs to Midbrain Dopamine Neurons , 2012, Neuron.

[46]  P. Redgrave,et al.  Functional properties of the basal ganglia's re-entrant loop architecture: selection and reinforcement , 2011, Neuroscience.

[47]  KouichiC . Nakamura,et al.  Expression of gap junction protein connexin36 in multiple subtypes of GABAergic neurons in adult rat somatosensory cortex. , 2011, Cerebral cortex.

[48]  F. Fujiyama,et al.  Exclusive and common targets of neostriatofugal projections of rat striosome neurons: a single neuron‐tracing study using a viral vector , 2011, The European journal of neuroscience.

[49]  H. Hioki,et al.  Coexpression of VGLUT1 and VGLUT2 in trigeminothalamic projection neurons in the principal sensory trigeminal nucleus of the rat , 2010, The Journal of comparative neurology.

[50]  F. Fujiyama,et al.  Vesicular glutamate transporter 3‐expressing nonserotonergic projection neurons constitute a subregion in the rat midbrain raphe nuclei , 2010, The Journal of comparative neurology.

[51]  E. Kuramoto,et al.  Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron-tracing study using viral vectors. , 2009, Cerebral cortex.

[52]  R. Rübsamen,et al.  Early Postnatal Development of Spontaneous and Acoustically Evoked Discharge Activity of Principal Cells of the Medial Nucleus of the Trapezoid Body: An In Vivo Study in Mice , 2009, The Journal of Neuroscience.

[53]  M. Deschenes,et al.  Septal neurons in barrel cortex derive their receptive field input from the lemniscal pathway , 2009, Neuroscience Research.

[54]  A. Nambu Seven problems on the basal ganglia , 2008, Current Opinion in Neurobiology.

[55]  Anatol C. Kreitzer,et al.  Striatal Plasticity and Basal Ganglia Circuit Function , 2008, Neuron.

[56]  M. Feller,et al.  Mechanisms underlying development of visual maps and receptive fields. , 2008, Annual review of neuroscience.

[57]  André Parent,et al.  Patterns of axonal branching of neurons of the substantia nigra pars reticulata and pars lateralis in the rat , 2005, The Journal of comparative neurology.

[58]  A. Parent,et al.  The striatofugal fiber system in primates: a reevaluation of its organization based on single-axon tracing studies. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[60]  Robert W. Williams,et al.  Complex trait analysis of the mouse striatum: independent QTLs modulate volume and neuron number , 2001, BMC Neuroscience.

[61]  A. Parent,et al.  The organization of the striatal output system: a single-cell juxtacellular labeling study in the rat , 2000, Neuroscience Research.

[62]  O. Hikosaka,et al.  Role of the basal ganglia in the control of purposive saccadic eye movements. , 2000, Physiological reviews.

[63]  M. Merello,et al.  [Functional anatomy of the basal ganglia]. , 2000, Revista de neurologia.

[64]  K. Johnson,et al.  Assessment of hearing in 80 inbred strains of mice by ABR threshold analyses , 1999, Hearing Research.

[65]  D. Pandya,et al.  Corticostriatal connections of the superior temporal region in rhesus monkeys , 1998, The Journal of comparative neurology.

[66]  S. Charpier,et al.  The lamellar organization of the rat substantia nigra pars reticulata: Segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections , 1996, Neuroscience.

[67]  V. Brown,et al.  Responses of cells in the tail of the caudate nucleus during visual discrimination learning. , 1995, Journal of neurophysiology.

[68]  M. Takada The lateroposterior thalamic nucleus and substantia nigra pars lateralis: Origin of dual innervation over the visual system and basal ganglia , 1992, Neuroscience Letters.

[69]  T. Hattori,et al.  Separate neuronal populations of the rat substantia nigra pars lateralis with distinct projection sites and transmitter phenotypes , 1992, Neuroscience.

[70]  K. Nakano,et al.  Non-dopaminergic projections from the substantia nigra pars lateralis to the inferior colliculus in the rat , 1991, Brain Research.

[71]  J. Hedreen,et al.  Organization of striatopallidal, striatonigral, and nigrostriatal projections in the macaque , 1991, The Journal of comparative neurology.

[72]  C. Wilson,et al.  Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[73]  Leslie G. Ungerleider,et al.  Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido‐nigral complex in the monkey , 1990, The Journal of comparative neurology.

[74]  Kenji Taniguchi,et al.  Direct and indirect transitions in (GaAs)n/(AlAs)n superlattices with n=1-15 , 1990, Other Conferences.

[75]  P. Goldman-Rakic,et al.  Topographic intermingling of striatonigral and striatopallidal neurons in the rhesus monkey , 1990, The Journal of comparative neurology.

[76]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[77]  A. Graybiel Neurotransmitters and neuromodulators in the basal ganglia , 1990, Trends in Neurosciences.

[78]  J. Penney,et al.  The functional anatomy of basal ganglia disorders , 1989, Trends in Neurosciences.

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

[80]  B. Kolb,et al.  The development of a patchy organization of the rat striatum. , 1986, Brain research.

[81]  S. Inagaki,et al.  Two distinct strio-nigral substance P pathways in the rat: An experimental immunohistochemical study , 1984, Brain Research.

[82]  E. T. Rolls,et al.  Responses of striatal neurons in the behaving monkey. 2. Visual processing in the caudal neostriatum , 1984, Brain Research.

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

[84]  G. Ehret Development of absolute auditory thresholds in the house mouse (Mus musculus). , 1976, Journal of the American Audiology Society.

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

[86]  Elsevier Biomedical Press RESPONSES OF STRIATAL NEURONS IN THE BEHAVING MONKEY. 1. HEAD OF THE CAUDATE NUCLEUS , 1983 .