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Defective Response Inhibition and Collicular Noradrenaline Enrichment Defective response inhibition and collicular noradrenaline enrichment in mice with duplicated retinotopic map in the superior colliculus Chantal Mathis, Élise Savier, Jean-Bastien Bott, Daniel Clesse, Nicholas Bevins, Dominique Ciocca, Karine Geiger, Anaïs Gillet, Alexis Laux-Biehlmann, Yannick Goumon, et al. To cite this version: Chantal Mathis, Élise Savier, Jean-Bastien Bott, Daniel Clesse, Nicholas Bevins, et al.. Defective response inhibition and collicular noradrenaline enrichment in mice with duplicated retinotopic map in the superior colliculus. Brain Structure and Function, Springer Verlag, 2014, 220 (3), pp.1573-1584. 10.1007/s00429-014-0745-5. hal-02884507 HAL Id: hal-02884507 https://hal.archives-ouvertes.fr/hal-02884507 Submitted on 3 Jul 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Brain Struct Funct (2015) 220:1573–1584 DOI 10.1007/s00429-014-0745-5 ORIGINAL ARTICLE Defective response inhibition and collicular noradrenaline enrichment in mice with duplicated retinotopic map in the superior colliculus Chantal Mathis • Elise Savier • Jean-Bastien Bott • Daniel Clesse • Nicholas Bevins • Dominique Sage-Ciocca • Karin Geiger • Anaı¨s Gillet • Alexis Laux-Biehlmann • Yannick Goumon • Adrien Lacaud • Vincent Lelie`vre • Christian Kelche • Jean-Christophe Cassel • Frank W. Pfrieger • Michael Reber Received: 5 February 2014 / Accepted: 28 February 2014 / Published online: 20 March 2014 Ó The Author(s) 2014. This article is published with open access at Springerlink.com Abstract The superior colliculus is a hub for multisen- performance of homozygous knock-in, heterozygous sory integration necessary for visuo-spatial orientation, knock-in and wild-type mice in several behavioral tasks control of gaze movements and attention. The multiple requiring collicular activity. The light/dark box test and functions of the superior colliculus have prompted Go/No-Go conditioning task revealed that homozygous hypotheses about its involvement in neuropsychiatric mutant mice exhibit defective response inhibition, a form conditions, but to date, this topic has not been addressed of impulsivity. This defect was specific to attention as other experimentally. We describe experiments on genetically tests showed no differences in visually driven behavior, modified mice, the Isl2-EphA3 knock-in line, that show a motivation, visuo-spatial learning and sensorimotor abili- well-characterized duplication of the retino-collicular and ties among the different groups of mice. Monoamine cortico-collicular axonal projections leading to hyperstim- quantification and gene expression profiling demonstrated a ulation of the superior colliculus. To explore the functional specific enrichment of noradrenaline only in the superficial impact of collicular hyperstimulation, we compared the layers of the superior colliculus of Isl2-EphA3 knock-in mice, where the retinotopy is duplicated, whereas transcript Electronic supplementary material The online version of this levels of receptors, transporters and metabolic enzymes of article (doi:10.1007/s00429-014-0745-5) contains supplementary the monoaminergic pathway were not affected. We dem- material, which is available to authorized users. onstrate that the defect in response inhibition is a conse- quence of noradrenaline imbalance in the superficial layers C. Mathis Á J.-B. Bott Á K. Geiger Á A. Gillet Á C. Kelche Á J.-C. Cassel of the superior colliculus caused by retinotopic map Laboratory of Adaptative and Cognitive Neurosciences, CNRS, duplication. Our results suggest that structural abnormali- University of Strasbourg UMR 7364, 67000 Strasbourg, France ties in the superior colliculus can cause defective response e-mail: [email protected] inhibition, a key feature of attention-deficit disorders. E. Savier Á D. Clesse Á A. Laux-Biehlmann Á Y. Goumon Á A. Lacaud Á V. Lelie`vre Á F. W. Pfrieger Á M. Reber (&) Keywords Retinotopy Á Visual system Á EphA signaling Á Institute of Cellular and Integrative Neurosciences, CNRS UPR Superior colliculus Á Noradrenaline Á Response inhibition Á 3212, University of Strasbourg, 5, rue blaise Pascal, Attention-deficit disorders 67084 Strasbourg, France e-mail: [email protected] N. Bevins Introduction Molecular Neurobiology Laboratory, The Salk Institute, La Jolla, San Diego, CA 92037, USA The superior colliculus (SC) is a midbrain structure that N. Bevins integrates sensory inputs from multiple modalities (Wal- Department of Neurosciences, University of California, La Jolla, lace et al. 1993; Holmes and Spence 2005; May 2006) and San Diego, CA 92039, USA plays a central role in visuo-spatial orientation, attention D. Sage-Ciocca and sensorimotor processing (Stein 1984; May 2006; Chronobiotron, UMS 3415, CNRS, 67084 Strasbourg, France Gandhi and Katnani 2011). Defects in SC function have 123 1574 Brain Struct Funct (2015) 220:1573–1584 Fig. 1 Topographic retino- collicular projections in WT and Isl2-EphA3KI animals. Micrographs illustrate nasal 1,10-dioctadecyl-3,3,3030- tetramethylindocarbocyanine perchlorate (Dil) injections in P8 retinas and the corresponding termination zone(s) in the SC. Top an injection in nasal WT retina leads to a single caudal termination zone in the SC. Middle an injection in a nasal EphA3KI/? retina leads to two caudal termination zones in the SC. Bottom an injection in a nasal EphA3KI/KI retina leads to two distant termination zones in the SC. Scale bars 1mm been associated with a number of neuropathological and collicular map (May 2006; Triplett et al. 2012). This cre- neuropsychiatric disorders including epilepsy (Ross and ates a topographic representation of the visual field in the Coleman 2000), schizophrenia (Fuentes 2001) and autism superficial layers of the SC, also called retinotopy. Audi- spectrum disorder (ASD) (Kleinhans et al. 2011). Recently, tory and somatosensory afferents projecting to deep layers collicular hyperstimulation has been proposed to underlie of the SC are also aligned with the visual maps (Meredith attention-deficit/hyperactivity disorder (ADHD) symptoms, and Stein 1985; King et al. 1998; May 2006) enhancing especially the impulsivity and distractibility associated perception of salient stimuli and influencing decision and with the disorder (Overton 2008; Miller 2009; Dommett overt behavior (Stein et al. 2009). et al. 2009). However, direct experimental evidence for We took advantage of a specific disruption of the reti- such a link remains elusive. notopy in the superficial layers of the SC that has been The SC presents a particular feature, namely the topo- observed in the Isl2-EphA3 knock-in mice (Fig. 1; Brown graphic organization of its sensory inputs (Sperry 1963; et al. 2000). In this mouse model, the EphA3 tyrosine Lemke and Reber 2005; May 2006). Axons of retinal kinase receptor, which acts as a guidance molecule during ganglion cells (RGCs) project to the superficial layers of map formation, is over-expressed by a subset of RGCs. the SC along spatial axes reflecting their position along This leads to a well-characterized duplication of the retino- corresponding axes in the retina (the retino-collicular map). collicular and cortico-collicular maps along the anterior– Layer V neurons of the V1 cortex also project in a topo- posterior axis of the SC. Over-expression of the EphA3 graphic manner to the superficial layers of the SC, the receptor neither affects retinal organization and integrity, cortico-collicular map, which is in register with the retino- nor the topography of collicular somatosensory inputs 123 Brain Struct Funct (2015) 220:1573–1584 1575 (Brown et al. 2000; Reber et al. 2004; Triplett et al. 2009; 67-358 for KG, AG was under their responsibility. Mice Bevins et al. 2011; Triplett et al. 2012). The duplicated were genotyped by PCR of genomic DNA from tail biop- visual maps are functional as single visual stimuli trigger sies as described previously (Reber et al. 2004). Four- to the activation of two distinct areas in the SC (Triplett et al. seven-month-old male littermates of each genotype 2009). Unlike other mouse models that target Eph/ephrin (EphA3KI/KI, EphA3KI/? and WT) on a mixed genetic signaling (Dottori et al. 1998; Feldheim et al. 2000; Feld- background (C57/Bl6 9 129Sv/J) were subjected to heim 2004), the genetic modification in the Isl2-EphA3 behavioral tests and molecular analyses. Standard labora- knock-in mice affects only a subset of RGCs and does not tory rodent food and water were available ad libitum affect other structures in the brain (Brown et al. 2000; throughout all experiments, except for the Go/No-Go task, Reber et al. 2004, Thaler et al. 2004). for which all mice were kept at 85 % of their free-feeding To determine if hyperstimulation of the SC, due to weight. duplication of the retinotopic projections, influences col- licular-related behavior, wild-type (WT), heterozygous Behavioral tests (EphA3KI/?) and homozygous (EphA3KI/KI) Isl2-EphA3KI mice were subjected to a series of well-established
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