A comprehensive excitatory input map of the striatum reveals novel functional organization

The striatum integrates excitatory inputs from the cortex and the thalamus to control diverse functions. Although the striatum is thought to consist of sensorimotor, associative and limbic domains, their precise demarcations and whether additional functional subdivisions exist remain unclear. How striatal inputs are differentially segregated into each domain is also poorly understood. This study presents a comprehensive map of the excitatory inputs to the mouse striatum. The input patterns reveal boundaries between the known striatal domains. The most posterior striatum likely represents the 4th functional subdivision, and the dorsomedial striatum integrates highly heterogeneous, multimodal inputs. The complete thalamo-cortico-striatal loop is also presented, which reveals that the thalamic subregions innervated by the basal ganglia preferentially interconnect with motor-related cortical areas. Optogenetic experiments show the subregion-specific heterogeneity in the synaptic properties of striatal inputs from both the cortex and the thalamus. This projectome will guide functional studies investigating diverse striatal functions. DOI: http://dx.doi.org/10.7554/eLife.19103.001

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

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

[3]  Alexander S. Tolpygo,et al.  High-Throughput Method of Whole-Brain Sectioning, Using the Tape-Transfer Technique , 2015, PloS one.

[4]  Ling Fu,et al.  Whole-Brain Mapping of Inputs to Projection Neurons and Cholinergic Interneurons in the Dorsal Striatum , 2015, PloS one.

[5]  Hongkui Zeng,et al.  Neuroinformatics of the Allen Mouse Brain Connectivity Atlas. , 2015, Methods.

[6]  G. Shepherd,et al.  The neocortical circuit: themes and variations , 2015, Nature Neuroscience.

[7]  Partha P. Mitra,et al.  The Circuit Architecture of Whole Brains at the Mesoscopic Scale , 2014, Neuron.

[8]  B. Sabatini,et al.  A Direct Projection from Mouse Primary Visual Cortex to Dorsomedial Striatum , 2014, PloS one.

[9]  S. Haber,et al.  Estimates of Projection Overlap and Zones of Convergence within Frontal-Striatal Circuits , 2014, The Journal of Neuroscience.

[10]  Tianyi Mao,et al.  A comprehensive thalamocortical projection map at the mesoscopic level , 2014, Nature Neuroscience.

[11]  Allan R. Jones,et al.  A mesoscale connectome of the mouse brain , 2014, Nature.

[12]  Arthur W. Toga,et al.  Neural Networks of the Mouse Neocortex , 2014, Cell.

[13]  Stefan R. Pulver,et al.  Independent Optical Excitation of Distinct Neural Populations , 2014, Nature Methods.

[14]  T. Wichmann,et al.  The thalamostriatal system in normal and diseased states , 2014, Front. Syst. Neurosci..

[15]  K. Berridge.  Faculty Opinions recommendation of Differential innervation of direct- and indirect-pathway striatal projection neurons. , 2013 .

[16]  Mohan Pabba.  Evolutionary development of the amygdaloid complex , 2013, Front. Neuroanat..

[17]  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.

[18]  J. Bolam,et al.  Convergence of cortical and thalamic input to direct and indirect pathway medium spiny neurons in the striatum , 2013, Brain Structure and Function.

[19]  Shinya Yamamoto,et al.  Reward Value-Contingent Changes of Visual Responses in the Primate Caudate Tail Associated with a Visuomotor Skill , 2013, The Journal of Neuroscience.

[20]  Ian R. Wickersham,et al.  Convergent cortical innervation of striatal projection neurons , 2013, Nature Neuroscience.

[21]  Philippe Mailly,et al.  The Rat Prefrontostriatal System Analyzed in 3D: Evidence for Multiple Interacting Functional Units , 2013, The Journal of Neuroscience.

[22]  J. Bolam,et al.  Heterogeneous properties of central lateral and parafascicular thalamic synapses in the striatum , 2012, The Journal of physiology.

[23]  R. J. McDonald,et al.  Context, emotion, and the strategic pursuit of goals: interactions among multiple brain systems controlling motivated behavior , 2012, Front. Behav. Neurosci..

[24]  K. Ressler,et al.  Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder , 2012, Trends in Neurosciences.

[25]  P. Redgrave,et al.  Thalamic Contributions to Basal Ganglia-Related Behavioral Switching and Reinforcement , 2011, The Journal of Neuroscience.

[26]  Karel Svoboda,et al.  Long-Range Neuronal Circuits Underlying the Interaction between Sensory and Motor Cortex , 2011, Neuron.

[27]  F. Martínez-García,et al.  Amygdaloid Projections to the Ventral Striatum in Mice: Direct and Indirect Chemosensory Inputs to the Brain Reward System , 2011, Frontiers in Neuroanatomy.

[28]  Tianyi Mao,et al.  Inputs to the Dorsal Striatum of the Mouse Reflect the Parallel Circuit Architecture of the Forebrain , 2010, Front. Neuroanat..

[29]  Xin Jin,et al.  Start/stop signals emerge in nigrostriatal circuits during sequence learning , 2010, Nature.

[30]  A. Graybiel,et al.  Differential Dynamics of Activity Changes in Dorsolateral and Dorsomedial Striatal Loops during Learning , 2010, Neuron.

[31]  Farran Briggs,et al.  Organizing Principles of Cortical Layer 6 , 2009, Front. Neural Circuits.

[32]  Steven J. M. Jones,et al.  Circos: an information aesthetic for comparative genomics. , 2009, Genome research.

[33]  A. Dickinson,et al.  Parallel and interactive learning processes within the basal ganglia: Relevance for the understanding of addiction , 2009, Behavioural Brain Research.

[34]  B. Balleine,et al.  The integrative function of the basal ganglia in instrumental conditioning , 2009, Behavioural Brain Research.

[35]  Mathieu Bastian,et al.  Gephi: An Open Source Software for Exploring and Manipulating Networks , 2009, ICWSM.

[36]  S. Haber,et al.  The cortico-basal ganglia integrative network: The role of the thalamus , 2009, Brain Research Bulletin.

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

[38]  Richard S. J. Frackowiak,et al.  Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia , 2008, The Journal of Neuroscience.

[39]  D. James Surmeier,et al.  Corticostriatal and Thalamostriatal Synapses Have Distinctive Properties , 2008, The Journal of Neuroscience.

[40]  Roy M. Smeal,et al.  A rat brain slice preparation for characterizing both thalamostriatal and corticostriatal afferents , 2007, Journal of Neuroscience Methods.

[41]  S. Haber,et al.  Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning , 2006, The Journal of Neuroscience.

[42]  H. Yin,et al.  The role of the basal ganglia in habit formation , 2006, Nature Reviews Neuroscience.

[43]  R. Guillery,et al.  Exploring the Thalamus and Its Role in Cortical Function , 2005 .

[44]  B. Balleine,et al.  The role of the dorsomedial striatum in instrumental conditioning , 2005, The European journal of neuroscience.

[45]  G. Shepherd,et al.  Laminar and Columnar Organization of Ascending Excitatory Projections to Layer 2/3 Pyramidal Neurons in Rat Barrel Cortex , 2005, The Journal of Neuroscience.

[46]  Nikolaus R. McFarland,et al.  Thalamic Relay Nuclei of the Basal Ganglia Form Both Reciprocal and Nonreciprocal Cortical Connections, Linking Multiple Frontal Cortical Areas , 2002, The Journal of Neuroscience.

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

[48]  E. Callaway,et al.  Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons , 2000, Nature Neuroscience.

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

[50]  Garrett E. Alexander.  Basal ganglia , 1998 .

[51]  C. Wilson,et al.  Corticostriatal innervation of the patch and matrix in the rat neostriatum , 1996, The Journal of comparative neurology.

[52]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[53]  A M Graybiel,et al.  The basal ganglia and adaptive motor control. , 1994, Science.

[54]  C. Gerfen.  The neostriatal mosaic: multiple levels of compartmental organization , 1992, Trends in Neurosciences.

[55]  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.

[56]  J. Deniau,et al.  The lamellar organization of the rat substantia nigra pars reticulata: Distribution of projection neurons , 1992, Neuroscience.

[57]  A. Parent,et al.  Topography of the projection from the central complex of the thalamus to the sensorimotor striatal territory in monkeys , 1991, The Journal of comparative neurology.

[58]  R. S. Waters,et al.  Organization of the Mouse Motor Cortex Studied by Retrograde Tracing and Intracortical Microstimulation (ICMS) Mapping , 1991, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[59]  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.

[60]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[61]  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.

[62]  A Sakaguchi,et al.  Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  J. Veening,et al.  The topical organization of the afferents to the caudatoputamen of the rat. A horseradish peroxidase study , 1980, Neuroscience.

[64]  C. W. Ragsdale,et al.  Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

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

[66]  W. Precht.  The synaptic organization of the brain G.M. Shepherd, Oxford University Press (1975). 364 pp., £3.80 (paperback) , 1976, Neuroscience.

[67]  H. Künzle.  Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study inMacaca fascicularis , 1975, Brain Research.

[68]  C. Gerfen,et al.  The Basal Ganglia , 2015 .

[69]  Charles Watson,et al.  The Mouse Nervous System. , 2012 .

[70]  Charles R. Gerfen,et al.  The Neuroanatomical Organization of the Basal Ganglia , 2010 .

[71]  Kuei Yuan Tseng,et al.  Handbook of basal ganglia structure and function , 2010 .

[72]  R. Faull,et al.  The Basal Ganglia , 2004 .

[73]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[74]  G. Shepherd.  The Synaptic Organization of the Brain , 1979 .