Lack of social exploratory activation in male μ-opioid receptor KO mice in response to playback of female ultrasonic vocalizations

REFERENCES

• Allin , J. T. and Banks , E. M. 1972 . Functional aspects of ultrasound production by infant albino rats (Rattus norvegicus) . Animal Behaviour , 20 ( 1 ) : 175 – 185 .
   Google Scholar
• American Psychiatric Association . 2000 . Diagnostic and Statistical Manual of Mental Disorders , 4th , Washington, DC : APA . text revision
   Google Scholar
• Benton , D. and Nastiti , K. 1988 . The influence of psychotropic drugs on the ultrasonic calling of mouse pups . Psychopharmacology , 95 ( 1 ) : 99 – 102 .
   Google Scholar
• Carden , S. E. and Hofer , M. A. 1990a . Independence of benzodiazepine and opiate actions in the suppression of isolation distress in rat pups . Behavioral Neuroscience , 104 ( 1 ) : 160 – 166 .
   Google Scholar
• Carden , S. E. and Hofer , M. A. 1990b . Socially mediated reduction of isolation distress in rat pups can be blocked by naltrexone but not by RO 15-1788 . Behavioral Neuroscience , 104 ( 3 ) : 457 – 463 .
   Google Scholar
• Cirulli , F. , Santucci , D. , Laviola , G. , Alleva , E. and Levine , S. 1994 . Behavioral and hormonal responses to stress in the newborn mouse: Effects of maternal deprivation and chlordiazepoxide . Developmental Psychobiology , 27 ( 5 ) : 301 – 316 .
   Google Scholar
• Costantini , F. and D'Amato , F. R. 2006 . Ultrasonic vocalizations in mice and rats: Social contexts and functions . Acta Zoologica Sinica , 52 ( 4 ) : 619 – 633 .
   Google Scholar
• Craft , R. M. 2008 . Sex differences in analgesic, reinforcing, discriminative, and motoric effects of opioids . Experimental and Clinical Psychopharmacology , 16 ( 5 ) : 376 – 385 .
   Google Scholar
• Crawley , J. N. 2007 . Mouse behavioral assays relevant to the symptoms of autism . Brain Pathology , 17 ( 4 ) : 448 – 459 .
   Google Scholar
• D'Amato , F. R. and Moles , A. 2001 . Ultrasonic vocalizations as an index of social memory in female mice . Behavioral Neuroscience , 115 ( 4 ) : 834 – 840 .
   Google Scholar
• Depue , R. A. and Morrone-Strupinsky , J. V. 2005 . A neurobehavioral model of affilative bonding: Implications for conceptualizing a human trait of affiliation . Behavioral and Brain Sciences , 28 ( 3 ) : 313 – 350 .
   PubMed Web of Science ®Google Scholar
• Enard , W. , Gehre , S. , Hammerschmidt , K. , Hölter , S. M. , Blass , T. Somel , M. 2009 . A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice . Cell , 137 ( 5 ) : 961 – 971 .
   PubMed Web of Science ®Google Scholar
• Filliol , D. , Ghozland , S. , Chluba , J. , Martin , M. , Matthes , H. W. Simonin , F. 2000 . Mice deficient for delta- and mu-opioid receptors exhibit opposing alterations of emotional responses . Nature Genetics , 25 ( 2 ) : 195 – 200 .
   PubMed Web of Science ®Google Scholar
• Fish , E. W. , Sekinda , M. , Ferrari , P. F. , Dirks , A. and Miczek , K. A. 2000 . Distress vocalizations in maternally separated mouse pups: Modulation via 5-HT(1A), 5‐HT(1B) and GABA(A) receptors . Psychopharmacology , 149 ( 3 ) : 277 – 285 .
   Google Scholar
• Frith , U. and Happé , F. 1994 . Language and communication in autistic disorders . Philosophical Transactions of the Royal Society, Series B: Biological Sciences , 346 ( 1315 ) : 97 – 104 .
   PubMed Web of Science ®Google Scholar
• Fujita , E. , Tanabe , Y. , Shiota , A. , Ueda , M. , Suwa , K. Momoi , M. Y. 2008 . Ultrasonic vocalization impairment of Foxp2 (R552H) knockin mice related to speech-language disorder and abnormality of Purkinje cells . Proceedings of the National Academy of Sciences of the United States of America , 105 ( 8 ) : 3117 – 3122 .
   Google Scholar
• Gourbal , B. E. , Barthelemy , M. , Petit , G. and Gabrion , C. 2004 . Spectrographic analysis of the ultrasonic vocalisations of adult male and female BALB/c mice . Naturwissenschaften , 91 ( 8 ) : 381 – 385 .
   PubMedGoogle Scholar
• Groszer , M. , Keays , D. A. , Deacon , R. M. , de Bono , J. P. , Prasad-Mulcare , S. Gaub , S. 2008 . Impaired synaptic plasticity and motor learning in mice with a point mutation implicated in human speech deficits . Current Biology , 18 ( 5 ) : 354 – 362 .
   Google Scholar
• Hammerschmidt , K. , Radyushkin , K. , Ehrenreich , H. and Fischer , J. 2009 . Female mice respond to male ultrasonic ‘songs’ with approach behaviour . Biology Letters , 5 ( 5 ) : 589 – 592 .
   Google Scholar
• Jamot , L. , Matthes , H. W. , Simonin , F. , Kieffer , B. L. and Roder , J. C. 2003 . Differential involvement of the mu and kappa opioid receptors in spatial learning . Genes, Brain and Behavior , 2 ( 2 ) : 80 – 92 .
   Google Scholar
• Kehoe , P. and Blass , E. M. 1986 . Opioid-mediation of separation distress in 10-day-old rats: Reversal of stress with maternal stimuli . Developmental Psychobiology , 19 ( 4 ) : 385 – 398 .
   Google Scholar
• Knutson , B. , Burgdorf , J. and Panksepp , J. 1998 . Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats . Journal of Comparative Psychology , 112 ( 1 ) : 65 – 73 .
   PubMed Web of Science ®Google Scholar
• Le Merrer , J. , Becker , J. A. J. , Befort , K. and Kieffer , B. L. 2009 . Reward processing by the opioid system in the brain . Physiological Reviews , 89 ( 4 ) : 1379 – 1412 .
   PubMed Web of Science ®Google Scholar
• Lord , C. , Leventhal , B. L. and Cook , E. H. 2001 . Quantifying the phenotype in autism spectrum disorders . American Journal of Medical Genetics , 105 ( 1 ) : 36 – 38 .
   Google Scholar
• Lord , C. , Risi , S. , Dilavore , P. S. , Shulman , C. , Thurm , A. and Pickles , A. 2006 . Autism from 2 to 9 years of age . Archives of General Psychiatry , 63 ( 6 ) : 694 – 701 .
   PubMed Web of Science ®Google Scholar
• Losh , M. and Piven , J. 2007 . Social-cognition and the broad autism phenotype: Identifying genetically meaningful phenotypes . Journal of Child Psychology and Psychiatry and Allied Disciplines , 48 ( 1 ) : 105 – 112 .
   Google Scholar
• Maggio , J. C. and Whitney , G. 1985 . Ultrasonic vocalizing by adult female mice (Mus musculus) . Journal of Comparative Psychology , 99 ( 4 ) : 420 – 436 .
   Google Scholar
• Matthes , H. W. , Maldonado , R. , Simonin , F. , Valverde , O. , Slowe , S. Kitchen , I. 1996 . Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene . Nature , 383 ( 6603 ) : 819 – 823 .
   PubMed Web of Science ®Google Scholar
• McIntosh , T. K. , Barfield , R. J. and Geyer , L. A. 1978 . Ultrasonic vocalisations facilitate sexual behaviour in female rats . Nature , 272 ( 5649 ) : 163 – 164 .
   Google Scholar
• Moles , A. , Costantini , F. , Garbugino , L. , Zanettini , C. and D'Amato , F. R. 2007 . Ultrasonic vocalization emitted during dyadic interactions in female mice: A possible index of sociability? . Behavioural Brain Research , 182 ( 2 ) : 223 – 230 .
   Google Scholar
• Moles , A. and D'Amato , F. R. 2000 . Ultrasonic vocalization by female mice in the presence of a conspecifics carrying food cues . Animal Behaviour , 60 ( 5 ) : 689 – 694 .
   Google Scholar
• Moles , A. , Kieffer , B. L. and D'Amato , F. R. 2004 . Deficit in attachment behavior in mice lacking the μ-opioid receptor gene . Science , 304 ( 5679 ) : 1983 – 1986 .
   PubMed Web of Science ®Google Scholar
• Morris , R. G. , Garrud , P. , Rawlins , J. N. and O'Keefe , J. 1982 . Place navigation impaired in rats with hippocampal lesions . Nature , 297 ( 5868 ) : 681 – 683 .
   PubMed Web of Science ®Google Scholar
• Nastiti , K. , Benton , D. and Brain , P. F. 1991 . The effects of compounds acting at the benzodiazepine receptor complex on the ultrasonic calling of mouse pups . Behavioural Pharmacology , 2 ( 2 ) : 121 – 128 .
   Google Scholar
• Nyby , J. 1983 . Ultrasonic vocalizations during sex behavior of male house mice (Mus musculus): a description . Behavioral and Neural Biology , 39 ( 1 ) : 128 – 134 .
   Google Scholar
• Panksepp , J. 1979 . A neurochemical theory of autism . Trends in Neurosciences , 2 ( 2 ) : 174 – 177 .
   Google Scholar
• Panksepp , J. and Bishop , P. 1981 . An autoradiographic map of [3H]diprenorphine binding in rat brain: Effects of social interaction . Brain Research Bulletin , 7 ( 4 ) : 405 – 410 .
   Google Scholar
• Panksepp , J. , Herman , B. H. , Vilberg , T. , Bishop , P. and DeEskinazi , F. G. 1980 . Endogenous opioids and social behavior . Neuroscience and Biobehavioral Reviews , 4 ( 4 ) : 473 – 487 .
   PubMed Web of Science ®Google Scholar
• Panksepp , J. B. , Jochman , K. A. , Kim , J. U. , Koy , J. J. , Wilson , E. D. Chen , Q. 2007 . Affiliative behavior, ultrasonic communication and social reward are influenced by genetic variation in adolescent mice . PLoS ONE , 2 ( 4 ) : e351
   Google Scholar
• Panksepp , J. , Nelson , E. and Bekkedal , M. 1997 . Brain systems for the mediation of social separation-distress and social-reward . Annals of the New York Academy of Sciences , 807 ( 2 ) : 78 – 100 .
   Google Scholar
• Phillips , R. G. and LeDoux , J. E. 1992 . Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning . Behavioral Neuroscience , 106 ( 2 ) : 274 – 285 .
   PubMed Web of Science ®Google Scholar
• Pomerantz , S. M. , Nunez , A. A. and Bean , N. J. 1983 . Female behavior is affected by male ultrasonic vocalizations in house mice . Physiology and Behavior , 31 ( 1 ) : 91 – 96 .
   Google Scholar
• Sadananda , M. , Wöhr , M. and Schwarting , R. K. W. 2008 . Playback of 22-kHz and 50-kHz ultrasonic vocalizations induces differential c-fos expression in rat brain . Neuroscience Letters , 435 ( 1 ) : 17 – 23 .
   Google Scholar
• Sahley , T. L. and Panksepp , J. 1987 . Brain opioids and autism: An updated analysis of possible linkages . Journal of Autism and Developmental Disorders , 17 ( 2 ) : 201 – 216 .
   Google Scholar
• Sales , G. D. 1972 . Ultrasound and mating behaviour in rodents with some observations on other behavioural situations . Journal of Zoology , 168 ( 2 ) : 149 – 164 .
   Google Scholar
• Scattoni , M. L. , Gandhy , S. U. , Ricceri , L. and Crawley , J. N. 2008 . Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism . PLoS ONE , 3 ( 8 ) : e3067
   PubMedGoogle Scholar
• Sewell , G. D. 1970 . Ultrasonic communication in rodents . Nature , 227 ( 5256 ) : 410
   Google Scholar
• Shu , W. , Cho , J. Y. , Jiang , Y. , Zhang , M. , Weisz , D. Elder , G. A. 2005 . Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene . Proceedings of the National Academy of Sciences of the United States of America , 102 ( 27 ) : 9643 – 9648 .
   Google Scholar
• Takahashi , A. , Yap , J. J. , Bohager , D. Z. , Faccidomo , S. , Clayton , T. Cook , J. M. 2009 . Glutamatergic and GABAergic modulations of ultrasonic vocalizations during maternal separation distress in mouse pups . Psychopharmacology , 204 ( 1 ) : 61 – 71 .
   Google Scholar
• Vanderschuren , L. J. M. J. , Stein , E. A. , Wiegant , V. M. and Van Ree , J. M. 1995 . Social play alters regional brain opioid receptor binding in juvenile rats . Brain Research , 680 ( 1–2 ) : 148 – 156 .
   Google Scholar
• Volkmar , F. R. , Lord , C. , Bailey , A. , Schultz , R. T. and Klin , A. J. 2004 . Autism and pervasive developmental disorders . Journal of Child Psychology and Psychiatry and Allied Disciplines , 45 ( 1 ) : 135 – 170 .
   PubMed Web of Science ®Google Scholar
• White , N. R. , Prasad , M. , Barfield , R. J. and Nyby , J. G. 1998 . 40- and 70-kHz vocalizations of mice (Mus musculus) during copulation . Physiology and Behavior , 63 ( 4 ) : 467 – 473 .
   Google Scholar
• Whitney , G. , Coble , J. R. , Stockton , M. D. and Tilson , E. F. 1973 . Ultrasonic emissions: Do they facilitate courtship of mice? . Journal of Comparative and Physiological Psychology , 84 ( 3 ) : 445 – 452 .
   Google Scholar
• Wöhr , M. , Dahlhoff , M. , Wolf , E. , Holsboer , F. , Schwarting , R. K. and Wotjak , C. T. 2008 . Effects of genetic background, gender, and early environmental factors on isolation-induced ultrasonic calling in mouse pups: An embryo-transfer study . Behaviour Genetics , 38 ( 6 ) : 579 – 595 .
   PubMed Web of Science ®Google Scholar
• Wöhr , M. , Oddi , D. and D'Amato , F. R. 2010 . “ Effect of altricial pup ultrasonic vocalization on maternal behavior ” . In Handbook of mammalian vocalization: An integrative neuroscience approach , Edited by: Brudzynski , S. M. 159 – 166 . Amsterdam : Elsevier–Academic Press .
   Google Scholar
• Wöhr , M. and Schwarting , R. K. W. 2007 . Ultrasonic communication in rats: Can playback of 50-kHz calls induce approach behavior? . PLoS ONE , 2 ( 12 ) : e1365
   Google Scholar
• Wöhr , M. and Schwarting , R. K. W. 2008 . Maternal care, isolation-induced infant ultrasonic calling, and their relations to adult anxiety-related behavior in the rat . Behavioral Neuroscience , 122 ( 2 ) : 310 – 330 .
   Google Scholar
• Wöhr , M. and Schwarting , R. K. W. 2010a . “ Activation of limbic system structures by replay of ultrasonic vocalization in rats ” . In Handbook of mammalian vocalization: An integrative neuroscience approach , Edited by: Brudzynski , S. M. 113 – 124 . Amsterdam : Elsevier–Academic Press .
   Google Scholar
• Wöhr , M. and Schwarting , R. K. W. 2010b . Ultrasonic communication in rats: Effects of morphine and naloxone on vocal and behavioral responses to playback of 50-kHz vocalizations . Pharmacology Biochemistry and Behavior , 94 ( 2 ) : 285 – 295 .
   Google Scholar
• Zippelius , H. M. and Schleidt , W. M. 1956 . Ultraschall-Laute bei jungen Mäusen [Ultrasonic vocalizations of young mice] . Naturwissenschaften , 43 ( 21 ) : 502
   Google Scholar