Brain Structure and Function

, Volume 223, Issue 3, pp 1275–1296 | Cite as

Mapping GPR88-Venus illuminates a novel role for GPR88 in sensory processing

  • Aliza T. Ehrlich
  • Meriem Semache
  • Julie Bailly
  • Stefan Wojcik
  • Tanzil M. Arefin
  • Christine Colley
  • Christian Le Gouill
  • Florence Gross
  • Viktoriya Lukasheva
  • Mireille Hogue
  • Emmanuel Darcq
  • Laura-Adela Harsan
  • Michel Bouvier
  • Brigitte L. Kieffer
Original Article

Abstract

GPR88 is an orphan G-protein coupled receptor originally characterized as a striatal-enriched transcript and is a potential target for neuropsychiatric disorders. At present, gene knockout studies in the mouse have essentially focused on striatal-related functions and a comprehensive knowledge of GPR88 protein distribution and function in the brain is still lacking. Here, we first created Gpr88-Venus knock-in mice expressing a functional fluorescent receptor to fine-map GPR88 localization in the brain. The receptor protein was detected in neuronal soma, fibers and primary cilia depending on the brain region, and remarkably, whole-brain mapping revealed a yet unreported layer-4 cortical lamination pattern specifically in sensory processing areas. The unique GPR88 barrel pattern in L4 of the somatosensory cortex appeared 3 days after birth and persisted into adulthood, suggesting a potential function for GPR88 in sensory integration. We next examined Gpr88 knockout mice for cortical structure and behavioral responses in sensory tasks. Magnetic resonance imaging of live mice revealed abnormally high fractional anisotropy, predominant in somatosensory cortex and caudate putamen, indicating significant microstructural alterations in these GPR88-enriched areas. Further, behavioral analysis showed delayed responses in somatosensory-, visual- and olfactory-dependent tasks, demonstrating a role for GPR88 in the integration rather than perception of sensory stimuli. In conclusion, our data show for the first time a prominent role for GPR88 in multisensory processing. Because sensory integration is disrupted in many psychiatric diseases, our study definitely positions GPR88 as a target to treat mental disorders perhaps via activity on cortical sensory networks.

Keywords

Orphan G protein-coupled receptor Gpr88 Knock-in and knockout mice Gpr88-Venus fluorescent protein Layer 4 cortex Primary cilia 

Notes

Acknowledgements

This work was supported by CQDM/Region Alsace/EU to BLK & MB, the US National Institute of Health (National Institute of Drug Abuse Grant no. 05010 to BLK and National Institute on Alcohol Abuse and Alcoholism, Grant no. 16658 to BLK), the Canada Fund for Innovation and the Canada Research Chairs to BLK and MB, and the Canadian Institute for Health Research (Grant no. MOP-10501 to MB). Conception and design of experiments were performed by ATE, JB, MS, LH, BLK, MB. Acquisition of data were performed by ATE, MS, JB, SW, TMA, CC, FG. Analysis of data were contributed by ATE, MS, FG, JB, TMA and ED. Design of tools or reagents was performed by CL, MH and VL. The original manuscript was written by ATE, ED and BLK. Revising and editing of the manuscript was done by ATE, BLK, ED, MS, TMA, LH, MB. We acknowledge Josée Prud’homme for preparation of human tissue specimens and the Douglas–Bell Canada Brain Bank that is supported by the Quebec Suicide Research Network of the Fonds de Recherche du Québec-Santé (FRQS) and by the Douglas Institute Foundation. The present study used the services of the Molecular and Cellular Microscopy Platform at the Douglas Hospital and Research Center. We would like to thank Monique Lagace for helpful discussions on the use of BRET biosensors. We also thank the mouse clinic institute (Illkirch, France) for mouse generation. We thank Aude Villemain, Eujin Kim and Aimee Lee Luco for animal care and genotyping. We thank the staff at the animal facility of the Neurophenotyping Center Douglas Hospital Research Center for the housing and maintenance of the animals.

Compliance with ethical standards

Conflict of interest

The authors report no potential conflict of interest.

Supplementary material

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References

  1. Alkufri F, Shaag A, Abu-Libdeh B, Elpeleg O (2016) Deleterious mutation in GPR88 is associated with chorea, speech delay, and learning disabilities. Neurol Genet 2(3):e64.  https://doi.org/10.1212/NXG.0000000000000064 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Arbuckle EP, Smith GD, Gomez MC, Lugo JN (2015) Testing for odor discrimination and habituation in mice. J Vis Exp 99:e52615.  https://doi.org/10.3791/52615 Google Scholar
  3. Arefin T, Mechling AE, Meirsman CA, Bienert T, Huebner NS, Lee HL, Ben Hamida S, Ehrlich A, Roquet D, Hennig J, von Elverfeldt D, Kieffer BL, Harsan LA (2017) Remodeling of sensorimotor brain connectivity in Gpr88 deficient mice. Brain Connect.  https://doi.org/10.1089/brain.2017.0486 PubMedGoogle Scholar
  4. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD (2005) Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45(2):207–221.  https://doi.org/10.1016/j.neuron.2004.12.036 CrossRefPubMedGoogle Scholar
  5. Badgandi HB, Hwang SH, Shimada IS, Loriot E, Mukhopadhyay S (2017) Tubby family proteins are adapters for ciliary trafficking of integral membrane proteins. J Cell Biol 216(3):743–760.  https://doi.org/10.1083/jcb.201607095 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Becker JA, Befort K, Blad C, Filliol D, Ghate A, Dembele D, Thibault C, Koch M, Muller J, Lardenois A, Poch O, Kieffer BL (2008) Transcriptome analysis identifies genes with enriched expression in the mouse central extended amygdala. Neuroscience 156(4):950–965.  https://doi.org/10.1016/j.neuroscience.2008.07.070 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Befort K, Filliol D, Ghate A, Darcq E, Matifas A, Muller J, Lardenois A, Thibault C, Dembele D, Le Merrer J, Becker JA, Poch O, Kieffer BL (2008) Mu-opioid receptor activation induces transcriptional plasticity in the central extended amygdala. Eur J Neurosci 27(11):2973–2984.  https://doi.org/10.1111/j.1460-9568.2008.06273.x CrossRefPubMedGoogle Scholar
  8. Berbari NF, Johnson AD, Lewis JS, Askwith CC, Mykytyn K (2008) Identification of ciliary localization sequences within the third intracellular loop of G protein-coupled receptors. Mol Biol Cell 19(4):1540–1547.  https://doi.org/10.1091/mbc.E07-09-0942 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bi YP (NJ, US), Dzierba, Carolyn Diane (Middletown, CT, US), Bronson, Joanne J. (Durham, CT, US), Fink, Cynthia (Lebanon, NJ, US), Green, Michael (Easton, PA, US), Kimball, David (East Windsor, NJ, US), Macor, John E. (Gullford, CT, US), Kwon, Soojin, Zhang, Yulian, Zipp, Greg (2013) Modulators of G protein-coupled receptor 88. United States PatentGoogle Scholar
  10. Braff DL, Geyer MA, Light GA, Sprock J, Perry W, Cadenhead KS, Swerdlow NR (2001) Impact of prepulse characteristics on the detection of sensorimotor gating deficits in schizophrenia. Schizophr Res 49(1–2):171–178CrossRefPubMedGoogle Scholar
  11. Brandish PE, Su M, Holder DJ, Hodor P, Szumiloski J, Kleinhanz RR, Forbes JE, McWhorter ME, Duenwald SJ, Parrish ML, Na S, Liu Y, Phillips RL, Renger JJ, Sankaranarayanan S, Simon AJ, Scolnick EM (2005) Regulation of gene expression by lithium and depletion of inositol in slices of adult rat cortex. Neuron 45(6):861–872.  https://doi.org/10.1016/j.neuron.2005.02.006 CrossRefPubMedGoogle Scholar
  12. Brown LL, Hand PJ, Divac I (1996) Representation of a single vibrissa in the rat neostriatum: peaks of energy metabolism reveal a distributed functional module. Neuroscience 75(3):717–728CrossRefPubMedGoogle Scholar
  13. Caspary T, Marazziti D, Berbari NF (2016) Methods for visualization of neuronal cilia. Methods Mol Biol 1454:203–214.  https://doi.org/10.1007/978-1-4939-3789-9_13 CrossRefPubMedGoogle Scholar
  14. Chen X, Luo J, Leng Y, Yang Y, Zweifel LS, Palmiter RD, Storm DR (2016) Ablation of type III adenylyl cyclase in mice causes reduced neuronal activity, altered sleep pattern, and depression-like phenotypes. Biol Psychiatry 80(11):836–848.  https://doi.org/10.1016/j.biopsych.2015.12.012 CrossRefPubMedGoogle Scholar
  15. Conti B, Maier R, Barr AM, Morale MC, Lu X, Sanna PP, Bilbe G, Hoyer D, Bartfai T (2007) Region-specific transcriptional changes following the three antidepressant treatments electro convulsive therapy, sleep deprivation and fluoxetine. Mol Psychiatry 12(2):167–189.  https://doi.org/10.1038/sj.mp.4001897 CrossRefPubMedGoogle Scholar
  16. Crandall SR, Cruikshank SJ, Connors BW (2015) A corticothalamic switch: controlling the thalamus with dynamic synapses. Neuron 86(3):768–782.  https://doi.org/10.1016/j.neuron.2015.03.040 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cudeiro J, Sillito AM (2006) Looking back: corticothalamic feedback and early visual processing. Trends Neurosci 29(6):298–306.  https://doi.org/10.1016/j.tins.2006.05.002 CrossRefPubMedGoogle Scholar
  18. Del Zompo M, Deleuze JF, Chillotti C, Cousin E, Niehaus D, Ebstein RP, Ardau R, Mace S, Warnich L, Mujahed M, Severino G, Dib C, Jordaan E, Murad I, Soubigou S, Koen L, Bannoura I, Rocher C, Laurent C, Derock M, Faucon Biguet N, Mallet J, Meloni R (2014) Association study in three different populations between the GPR88 gene and major psychoses. Mol Genet Genomic Med 2(2):152–159.  https://doi.org/10.1002/mgg3.54 CrossRefPubMedGoogle Scholar
  19. Divac I, Rosvold HE, Szwarcbart MK (1967) Behavioral effects of selective ablation of the caudate nucleus. J Comp Physiol Psychol 63(2):184–190CrossRefPubMedGoogle Scholar
  20. Dzierba CD, Bi Y, Dasgupta B, Hartz RA, Ahuja V, Cianchetta G, Kumi G, Dong L, Aleem S, Fink C, Garcia Y, Green M, Han J, Kwon S, Qiao Y, Wang J, Zhang Y, Liu Y, Zipp G, Liang Z, Burford N, Ferrante M, Bertekap R, Lewis M, Cacace A, Grace J, Wilson A, Nouraldeen A, Westphal R, Kimball D, Carson K, Bronson JJ, Macor JE (2015) Design, synthesis, and evaluation of phenylglycinols and phenyl amines as agonists of GPR88. Bioorg Med Chem Lett 25(7):1448–1452.  https://doi.org/10.1016/j.bmcl.2015.01.036 CrossRefPubMedGoogle Scholar
  21. Erbs E, Faget L, Veinante P, Kieffer BL, Massotte D (2014) In vivo neuronal co-expression of mu and delta opioid receptors uncovers new therapeutic perspectives. Recept Clin Investig.  https://doi.org/10.14800/rci.210 Google Scholar
  22. Erbs E, Faget L, Scherrer G, Matifas A, Filliol D, Vonesch JL, Koch M, Kessler P, Hentsch D, Birling MC, Koutsourakis M, Vasseur L, Veinante P, Kieffer BL, Massotte D (2015) A mu-delta opioid receptor brain atlas reveals neuronal co-occurrence in subcortical networks. Brain Struct Funct 220(2):677–702.  https://doi.org/10.1007/s00429-014-0717-9 CrossRefPubMedGoogle Scholar
  23. Faget L, Erbs E, Le Merrer J, Scherrer G, Matifas A, Benturquia N, Noble F, Decossas M, Koch M, Kessler P, Vonesch JL, Schwab Y, Kieffer BL, Massotte D (2012) In vivo visualization of delta opioid receptors upon physiological activation uncovers a distinct internalization profile. J Neurosci 32(21):7301–7310.  https://doi.org/10.1523/JNEUROSCI.0185-12.2012 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Feldmeyer D (2012) Excitatory neuronal connectivity in the barrel cortex. Front Neuroanat 6:24.  https://doi.org/10.3389/fnana.2012.00024 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ferezou I, Haiss F, Gentet LJ, Aronoff R, Weber B, Petersen CC (2007) Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56(5):907–923.  https://doi.org/10.1016/j.neuron.2007.10.007 CrossRefPubMedGoogle Scholar
  26. Fishell G, van der Kooy D (1989) Pattern formation in the striatum: developmental changes in the distribution of striatonigral projections. Brain Res Dev Brain Res 45(2):239–255CrossRefPubMedGoogle Scholar
  27. Fleige S, Pfaffl MW (2006) RNA integrity and the effect on the real-time qRT-PCR performance. Mol Aspects Med 27(2–3):126–139.  https://doi.org/10.1016/j.mam.2005.12.003 CrossRefPubMedGoogle Scholar
  28. Fox MW (1965) The visual cliff test for the study of visual depth perception in the mouse. Anim Behav 13(2):232–233CrossRefPubMedGoogle Scholar
  29. Gardon O, Faget L, Chu Sin Chung P, Matifas A, Massotte D, Kieffer BL (2014) Expression of mu opioid receptor in dorsal diencephalic conduction system: new insights for the medial habenula. Neuroscience 277:595–609.  https://doi.org/10.1016/j.neuroscience.2014.07.053 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Ghate A, Befort K, Becker JA, Filliol D, Bole-Feysot C, Demebele D, Jost B, Koch M, Kieffer BL (2007) Identification of novel striatal genes by expression profiling in adult mouse brain. Neuroscience 146(3):1182–1192.  https://doi.org/10.1016/j.neuroscience.2007.02.040 CrossRefPubMedGoogle Scholar
  31. Guemez-Gamboa A, Coufal NG, Gleeson JG (2014) Primary cilia in the developing and mature brain. Neuron 82(3):511–521.  https://doi.org/10.1016/j.neuron.2014.04.024 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Guo ZV, Li N, Huber D, Ophir E, Gutnisky D, Ting JT, Feng G, Svoboda K (2014) Flow of cortical activity underlying a tactile decision in mice. Neuron 81(1):179–194.  https://doi.org/10.1016/j.neuron.2013.10.020 CrossRefPubMedGoogle Scholar
  33. Harsan LA, David C, Reisert M, Schnell S, Hennig J, von Elverfeldt D, Staiger JF (2013) Mapping remodeling of thalamocortical projections in the living reeler mouse brain by diffusion tractography. Proc Natl Acad Sci USA 110(19):E1797–E1806.  https://doi.org/10.1073/pnas.1218330110 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Hodges A, Strand AD, Aragaki AK, Kuhn A, Sengstag T, Hughes G, Elliston LA, Hartog C, Goldstein DR, Thu D, Hollingsworth ZR, Collin F, Synek B, Holmans PA, Young AB, Wexler NS, Delorenzi M, Kooperberg C, Augood SJ, Faull RL, Olson JM, Jones L, Luthi-Carter R (2006) Regional and cellular gene expression changes in human Huntington’s disease brain. Hum Mol Genet 15(6):965–977.  https://doi.org/10.1093/hmg/ddl013 CrossRefPubMedGoogle Scholar
  35. Ingallinesi M, Le Bouil L, Biguet NF, Thi AD, Mannoury la Cour C, Millan MJ, Ravassard P, Mallet J, Meloni R (2015) Local inactivation of Gpr88 in the nucleus accumbens attenuates behavioral deficits elicited by the neonatal administration of phencyclidine in rats. Mol Psychiatry 20(8):951–958.  https://doi.org/10.1038/mp.2014.92 CrossRefPubMedGoogle Scholar
  36. Jin C, Decker AM, Huang XP, Gilmour BP, Blough BE, Roth BL, Hu Y, Gill JB, Zhang XP (2014) Synthesis, pharmacological characterization, and structure-activity relationship studies of small molecular agonists for the orphan GPR88 receptor. ACS Chem Neurosci 5(7):576–587.  https://doi.org/10.1021/cn500082p CrossRefPubMedPubMedCentralGoogle Scholar
  37. Jin C, Decker AM, Langston TL (2017) Design, synthesis and pharmacological evaluation of 4-hydroxyphenylglycine and 4-hydroxyphenylglycinol derivatives as GPR88 agonists. Bioorg Med Chem 25(2):805–812.  https://doi.org/10.1016/j.bmc.2016.11.058 CrossRefPubMedGoogle Scholar
  38. Kumamoto N, Gu Y, Wang J, Janoschka S, Takemaru K, Levine J, Ge S (2012) A role for primary cilia in glutamatergic synaptic integration of adult-born neurons. Nat Neurosci 15(3):399–405, S391v.  https://doi.org/10.1038/nn.3042 CrossRefGoogle Scholar
  39. Le Merrer J, Befort K, Gardon O, Filliol D, Darcq E, Dembele D, Becker JA, Kieffer BL (2012) Protracted abstinence from distinct drugs of abuse shows regulation of a common gene network. Addict Biol 17(1):1–12.  https://doi.org/10.1111/j.1369-1600.2011.00365.x CrossRefPubMedGoogle Scholar
  40. Li JX, Thorn DA, Jin C (2013) The GPR88 receptor agonist 2-PCCA does not alter the behavioral effects of methamphetamine in rats. Eur J Pharmacol 698(1–3):272–277.  https://doi.org/10.1016/j.ejphar.2012.10.037 CrossRefPubMedGoogle Scholar
  41. Liguz-Lecznar M, Zakrzewska R, Daniszewska K, Kossut M (2014) Functional assessment of sensory functions after photothrombotic stroke in the barrel field of mice. Behav Brain Res 261:202–209.  https://doi.org/10.1016/j.bbr.2013.12.027 CrossRefPubMedGoogle Scholar
  42. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefPubMedGoogle Scholar
  43. Logue SF, Grauer SM, Paulsen J, Graf R, Taylor N, Sung MA, Zhang L, Hughes Z, Pulito VL, Liu F, Rosenzweig-Lipson S, Brandon NJ, Marquis KL, Bates B, Pausch M (2009) The orphan GPCR, GPR88, modulates function of the striatal dopamine system: a possible therapeutic target for psychiatric disorders? Mol Cell Neurosci 42(4):438–447.  https://doi.org/10.1016/j.mcn.2009.09.007 CrossRefPubMedGoogle Scholar
  44. Ludewig K, Geyer MA, Etzensberger M, Vollenweider FX (2002) Stability of the acoustic startle reflex, prepulse inhibition, and habituation in schizophrenia. Schizophr Res 55(1–2):129–137CrossRefPubMedGoogle Scholar
  45. Mai JK, Voss T, Paxinos G (2008) Atlas of the human brain, 3rd edn. Elsevier/Academic Press, AmsterdamGoogle Scholar
  46. Maier DL, Mani S, Donovan SL, Soppet D, Tessarollo L, McCasland JS, Meiri KF (1999) Disrupted cortical map and absence of cortical barrels in growth-associated protein (GAP)-43 knockout mice. Proc Natl Acad Sci USA 96(16):9397–9402CrossRefPubMedPubMedCentralGoogle Scholar
  47. Manita S, Suzuki T, Homma C, Matsumoto T, Odagawa M, Yamada K, Ota K, Matsubara C, Inutsuka A, Sato M, Ohkura M, Yamanaka A, Yanagawa Y, Nakai J, Hayashi Y, Larkum ME, Murayama M (2015) A top-down cortical circuit for accurate sensory perception. Neuron 86(5):1304–1316.  https://doi.org/10.1016/j.neuron.2015.05.006 CrossRefPubMedGoogle Scholar
  48. Marley A, Choy RW, von Zastrow M (2013) GPR88 reveals a discrete function of primary cilia as selective insulators of GPCR cross-talk. PLoS One 8(8):e70857.  https://doi.org/10.1371/journal.pone.0070857 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Massart R, Guilloux JP, Mignon V, Sokoloff P, Diaz J (2009) Striatal GPR88 expression is confined to the whole projection neuron population and is regulated by dopaminergic and glutamatergic afferents. Eur J Neurosci 30(3):397–414.  https://doi.org/10.1111/j.1460-9568.2009.06842.x CrossRefPubMedGoogle Scholar
  50. Massart R, Mignon V, Stanic J, Munoz-Tello P, Becker JA, Kieffer BL, Darmon M, Sokoloff P, Diaz J (2016) Developmental and adult expression patterns of the G-protein-coupled receptor GPR88 in the rat: establishment of a dual nuclear-cytoplasmic localization. J Comp Neurol 524(14):2776–2802.  https://doi.org/10.1002/cne.23991 CrossRefPubMedGoogle Scholar
  51. Masuho I, Ostrovskaya O, Kramer GM, Jones CD, Xie K, Martemyanov KA (2015) Distinct profiles of functional discrimination among G proteins determine the actions of G protein-coupled receptors. Sci Signal 8(405):ra123.  https://doi.org/10.1126/scisignal.aab4068 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Meirsman AC, Le Merrer J, Pellissier LP, Diaz J, Clesse D, Kieffer BL, Becker JA (2016a) Mice lacking GPR88 show motor deficit, improved spatial learning, and low anxiety reversed by delta opioid antagonist. Biol Psychiatry 79(11):917–927.  https://doi.org/10.1016/j.biopsych.2015.05.020 CrossRefPubMedGoogle Scholar
  53. Meirsman AC, Robe A, de Kerchove d’Exaerde A, Kieffer BL (2016b) GPR88 in A2AR neurons enhances anxiety-like behaviors. eNeuro.  https://doi.org/10.1523/ENEURO.0202-16.2016 PubMedPubMedCentralGoogle Scholar
  54. Meirsman AC, de Kerchove d’Exaerde A, Kieffer BL, Ouagazzal AM (2017) GPR88 in A2A receptor-expressing neurons modulates locomotor response to dopamine agonists but not sensorimotor gating. Eur J Neurosci 46(4):2026–2034.  https://doi.org/10.1111/ejn.13646 CrossRefPubMedGoogle Scholar
  55. Metz GA, Schwab ME (2004) Behavioral characterization in a comprehensive mouse test battery reveals motor and sensory impairments in growth-associated protein-43 null mutant mice. Neuroscience 129(3):563–574.  https://doi.org/10.1016/j.neuroscience.2004.07.053 CrossRefPubMedGoogle Scholar
  56. Mizushima K, Miyamoto Y, Tsukahara F, Hirai M, Sakaki Y, Ito T (2000) A novel G-protein-coupled receptor gene expressed in striatum. Genomics 69(3):314–321.  https://doi.org/10.1006/geno.2000.6340 CrossRefPubMedGoogle Scholar
  57. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8(6):427–437.  https://doi.org/10.1038/nrn2151 CrossRefPubMedGoogle Scholar
  58. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20(1):87–90.  https://doi.org/10.1038/nbt0102-87 CrossRefPubMedGoogle Scholar
  59. Nagy A, Paroczy Z, Norita M, Benedek G (2005) Multisensory responses and receptive field properties of neurons in the substantia nigra and in the caudate nucleus. Eur J Neurosci 22(2):419–424.  https://doi.org/10.1111/j.1460-9568.2005.04211.x CrossRefPubMedGoogle Scholar
  60. Niell CM (2015) Cell types, circuits, and receptive fields in the mouse visual cortex. Annu Rev Neurosci 38:413–431.  https://doi.org/10.1146/annurev-neuro-071714-033807 CrossRefPubMedGoogle Scholar
  61. Nieto M, Monuki ES, Tang H, Imitola J, Haubst N, Khoury SJ, Cunningham J, Gotz M, Walsh CA (2004) Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J Comp Neurol 479(2):168–180.  https://doi.org/10.1002/cne.20322 CrossRefPubMedGoogle Scholar
  62. Ogden CA, Rich ME, Schork NJ, Paulus MP, Geyer MA, Lohr JB, Kuczenski R, Niculescu AB (2004) Candidate genes, pathways and mechanisms for bipolar (manic-depressive) and related disorders: an expanded convergent functional genomics approach. Mol Psychiatry 9(11):1007–1029.  https://doi.org/10.1038/sj.mp.4001547 CrossRefPubMedGoogle Scholar
  63. Perry W, Minassian A, Feifel D, Braff DL (2001) Sensorimotor gating deficits in bipolar disorder patients with acute psychotic mania. Biol Psychiatry 50(6):418–424CrossRefPubMedGoogle Scholar
  64. Powell SB, Weber M, Geyer MA (2012) Genetic models of sensorimotor gating: relevance to neuropsychiatric disorders. Curr Top Behav Neurosci 12:251–318.  https://doi.org/10.1007/7854_2011_195 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Pradhan AA, Becker JA, Scherrer G, Tryoen-Toth P, Filliol D, Matifas A, Massotte D, Gaveriaux-Ruff C, Kieffer BL (2009) In vivo delta opioid receptor internalization controls behavioral effects of agonists. PLoS One 4(5):e5425.  https://doi.org/10.1371/journal.pone.0005425 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Pradhan AA, Walwyn W, Nozaki C, Filliol D, Erbs E, Matifas A, Evans C, Kieffer BL (2010) Ligand-directed trafficking of the delta-opioid receptor in vivo: two paths toward analgesic tolerance. J Neurosci 30(49):16459–16468.  https://doi.org/10.1523/JNEUROSCI.3748-10.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Pradhan AA, Befort K, Nozaki C, Gaveriaux-Ruff C, Kieffer BL (2011) The delta opioid receptor: an evolving target for the treatment of brain disorders. Trends Pharmacol Sci 32(10):581–590.  https://doi.org/10.1016/j.tips.2011.06.008 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Quintana A, Sanz E, Wang W, Storey GP, Guler AD, Wanat MJ, Roller BA, La Torre A, Amieux PS, McKnight GS, Bamford NS, Palmiter RD (2012) Lack of GPR88 enhances medium spiny neuron activity and alters motor- and cue-dependent behaviors. Nat Neurosci 15(11):1547–1555.  https://doi.org/10.1038/nn.3239 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Reig R, Silberberg G (2014) Multisensory integration in the mouse striatum. Neuron 83(5):1200–1212.  https://doi.org/10.1016/j.neuron.2014.07.033 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Rezai X, Faget L, Bednarek E, Schwab Y, Kieffer BL, Massotte D (2012) Mouse delta opioid receptors are located on presynaptic afferents to hippocampal pyramidal cells. Cell Mol Neurobiol 32(4):509–516.  https://doi.org/10.1007/s10571-011-9791-1 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Schallert T, Whishaw IQ (1984) Bilateral cutaneous stimulation of the somatosensory system in hemidecorticate rats. Behav Neurosci 98(3):518–540CrossRefPubMedGoogle Scholar
  72. Scherrer G, Tryoen-Toth P, Filliol D, Matifas A, Laustriat D, Cao YQ, Basbaum AI, Dierich A, Vonesh JL, Gaveriaux-Ruff C, Kieffer BL (2006) Knockin mice expressing fluorescent delta-opioid receptors uncover G protein-coupled receptor dynamics in vivo. Proc Natl Acad Sci USA 103(25):9691–9696.  https://doi.org/10.1073/pnas.0603359103 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Scherrer G, Imamachi N, Cao YQ, Contet C, Mennicken F, O’Donnell D, Kieffer BL, Basbaum AI (2009) Dissociation of the opioid receptor mechanisms that control mechanical and heat pain. Cell 137(6):1148–1159.  https://doi.org/10.1016/j.cell.2009.04.019 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Schneider DM, Nelson A, Mooney R (2014) A synaptic and circuit basis for corollary discharge in the auditory cortex. Nature 513(7517):189–194.  https://doi.org/10.1038/nature13724 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Schulz JM, Redgrave P, Mehring C, Aertsen A, Clements KM, Wickens JR, Reynolds JN (2009) Short-latency activation of striatal spiny neurons via subcortical visual pathways. J Neurosci 29(19):6336–6347.  https://doi.org/10.1523/JNEUROSCI.4815-08.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Song DD, Harlan RE (1994) Genesis and migration patterns of neurons forming the patch and matrix compartments of the rat striatum. Brain Res Dev Brain Res 83(2):233–245CrossRefPubMedGoogle Scholar
  77. Swerdlow NR, Lipska BK, Weinberger DR, Braff DL, Jaskiw GE, Geyer MA (1995) Increased sensitivity to the sensorimotor gating-disruptive effects of apomorphine after lesions of medial prefrontal cortex or ventral hippocampus in adult rats. Psychopharmacology 122(1):27–34CrossRefPubMedGoogle Scholar
  78. Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL (2008) Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology 199(3):331–388.  https://doi.org/10.1007/s00213-008-1072-4 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Van der Loos H, Woolsey TA (1973) Somatosensory cortex: structural alterations following early injury to sense organs. Science 179(4071):395–398CrossRefPubMedGoogle Scholar
  80. Van Waes V, Tseng KY, Steiner H (2011) GPR88—a putative signaling molecule predominantly expressed in the striatum: cellular localization and developmental regulation. Basal Ganglia 1(2):83–89.  https://doi.org/10.1016/j.baga.2011.04.001 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Vassilatis DK, Hohmann JG, Zeng H, Li F, Ranchalis JE, Mortrud MT, Brown A, Rodriguez SS, Weller JR, Wright AC, Bergmann JE, Gaitanaris GA (2003) The G protein-coupled receptor repertoires of human and mouse. Proc Natl Acad Sci USA 100(8):4903–4908.  https://doi.org/10.1073/pnas.0230374100 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wilson CJ (2014) The sensory striatum. Neuron 83(5):999–1001.  https://doi.org/10.1016/j.neuron.2014.08.025 CrossRefPubMedGoogle Scholar
  83. Wilson JS, Hull CD, Buchwald NA (1983) Intracellular studies of the convergence of sensory input on caudate neurons of cat. Brain Res 270(2):197–208CrossRefPubMedGoogle Scholar
  84. Yang M, Crawley JN (2009) Simple behavioral assessment of mouse olfaction. Curr Protoc Neurosci.  https://doi.org/10.1002/0471142301.ns0824s48 (Chapter 8) PubMedPubMedCentralGoogle Scholar
  85. Zembrzycki A, Chou SJ, Ashery-Padan R, Stoykova A, O’Leary DD (2013) Sensory cortex limits cortical maps and drives top-down plasticity in thalamocortical circuits. Nat Neurosci 16(8):1060–1067.  https://doi.org/10.1038/nn.3454 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Zhang S, Xu M, Kamigaki T, Hoang Do JP, Chang WC, Jenvay S, Miyamichi K, Luo L, Dan Y (2014) Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing. Science 345(6197):660–665.  https://doi.org/10.1126/science.1254126 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Aliza T. Ehrlich
    • 1
    • 6
  • Meriem Semache
    • 2
  • Julie Bailly
    • 1
  • Stefan Wojcik
    • 1
    • 9
  • Tanzil M. Arefin
    • 3
    • 4
    • 5
    • 6
  • Christine Colley
    • 1
    • 9
  • Christian Le Gouill
    • 2
  • Florence Gross
    • 1
    • 2
  • Viktoriya Lukasheva
    • 2
  • Mireille Hogue
    • 2
  • Emmanuel Darcq
    • 1
  • Laura-Adela Harsan
    • 3
    • 7
    • 8
  • Michel Bouvier
    • 2
  • Brigitte L. Kieffer
    • 1
    • 6
  1. 1.Department of PsychiatryMcGill University, Douglas Hospital Research CenterMontrealCanada
  2. 2.Department of Biochemistry, Institute for Research in Immunology and CancerUniversité de MontréalMontréalCanada
  3. 3.Department of Radiology, Medical Physics, Medical Center University of Freiburg, Faculty of MedicineUniversity of FreiburgFreiburgGermany
  4. 4.Faculty of BiologyUniversity of FreiburgFreiburgGermany
  5. 5.Bernard and Irene Schwartz Center for Biomedical ImagingNew York University School of MedicineNew YorkUSA
  6. 6.Institut de Génétique et de Biologie Moléculaire et CellulaireIllkirch-GraffenstadenFrance
  7. 7.Engineering Science, Computer Science and Imaging Laboratory (ICube), Integrative Multimodal Imaging in HealthcareUniversity of Strasbourg, CNRSStrasbourgFrance
  8. 8.Department of Biophysics and Nuclear Medicine, Faculty of MedicineUniversity Hospital StrasbourgStrasbourgFrance
  9. 9.Department of Biochemical Sciences, Faculty of Health and Medical SciencesUniversity of SurreyGuildfordUK

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