Abstract
To examine processes underlying generational and developmental influences on anxiety, this laboratory produced two lines of (N:NIH strain) rats, selectively bred on the basis extreme rates of ultrasonic vocalization in 2 minutes of isolation at Postnatal Day 10. The research reviewed in this article focuses on: (1) establishment of the selectively bred lines; (2) defining infant behavioral and physiological phenotypes and (3) determining whether infantile USV phenotypes endure over development. The High and Low lines have diverged widely in their USV rates from each other and from the Random control line, which has maintained N:NIH strain rates overall from generation to generation. Beginning in the 11th generation, High USV pups have shown significantly higher frequencies of defecation and urination during isolation screening than the Low USV and random control line. Both lines show altered autonomic regulation of heart rates (HR) in response to stressors as juveniles and adults. These differences in HR responses in High and Low lines appear to be mediated by changes in the balance of sympathetic versus parasympathetic mechanisms. Other behavioral characteristics of the High line are consistent with an “anxious”/ “depressive” phenotype, such as vocalizations to touch in a novel environment, and performance in the Porsolt Swim, whereas Low line shows few differences in anxiety behavior. Future work will resolve the similarities and differences in the High and Low phenotypes and provide a developmental perspective to the growing body of information about affective regulation in humans and animals provided by selectively bred animal models.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
N. Ahmadiyeh G. A. Churchill K. Shimomura L. C. Solberg J. S. Takahashi E. E. Redei (2003) ArticleTitleX-linked and lineage-dependent inheritance of coping responses to stress Mamm. Genome. 14 748–757 Occurrence Handle10.1007/s00335-003-2292-x Occurrence Handle14722724
E. A. Antoniadis R. J. McDonald (1999) ArticleTitleDiscriminative fear conditioning to context expressed by multiple measures of fear in the rat Behav. Brain Res. 101 IssueID1 1–13 Occurrence Handle10.1016/S0166-4328(98)00056-4 Occurrence Handle10342394 Occurrence Handle1:STN:280:DyaK1M3ntFyhsA%3D%3D
J. Archer (1973) ArticleTitleTests for emotionality in rats and mice: a review Animal Behav. 21 IssueID2 205–235 Occurrence Handle1:STN:280:DyaE3s3is12qtg%3D%3D
G. G. Berntson J. T. Cacioppo K. S. Quigley V. T. Fabro (1994) ArticleTitleAutonomic space and psychophysiological response Behav. Brain Res. 62 11–20 Occurrence Handle10.1016/0166-4328(94)90033-7 Occurrence Handle7917029
J. Biederman D. R. Hirshfeld-Becker J. F. Rosenbaum C. Herot D. Friedman N. Snidman J. Kagam S. B. Faraone (2001) ArticleTitleFurther evidence of association between behavioral inhibition and social anxiety in children. Am. J. Psychiat. 158 IssueID10 1673–1679 Occurrence Handle10.1176/appi.ajp.158.10.1673 Occurrence Handle11579001 Occurrence Handle1:STN:280:DC%2BD3MrjtF2nsw%3D%3D
J. Biederman J. F. Rosenbaum M. A. Hirshfeld S. V. Faraone E. A. Bolduc E. Gersten (1990) ArticleTitlePsychiatric correlates of behavioral inhibition in young children of parents with and without psychiatric disorders Arch. General Psychiatr. 47 21–26 Occurrence Handle1:STN:280:DyaK3c7gtlyjtQ%3D%3D
J. Biederman J. F. Rosenbaum E. A. Bolduc-Murphy S. V. Faraone J. Chaloff D. R. Hirshfeld J. Kagan (1993) ArticleTitleA 3 -year follow-up of children with and without behavioral inhibition J. Am. Acad. Child Adol. Psychiatr. 32 814–821 Occurrence Handle1:STN:280:DyaK3szktVSitg%3D%3D
D. A. Blizard (1981) ArticleTitleThe Maudsley reactive and nonreactive strains: a North American perspective Behav. Genet. 11 IssueID5 469–489 Occurrence Handle7325951 Occurrence Handle1:STN:280:DyaL387htlSjtQ%3D%3D
D. A. Blizard N. Adams (2002) ArticleTitleThe Maudsley reactive and nonreactive strains: a new perspective Behav. Genet. 32 IssueID5 277–299 Occurrence Handle10.1023/A:1020206120248 Occurrence Handle12405512
B. F. Blok G. Holstege (1999) ArticleTitleThe central control of micturition and continence: implications for urology. BJU Int. 83 IssueIDsuppl 2 1–6 Occurrence Handle10.1046/j.1464-410X.83.s2.2.x Occurrence Handle10210596
J. Bowlby (1969) Attachment and loss Basic Books New York
BrudzynskiS. M. Principles of rat communication :quantitative parameters of ultrasonic calls in rats. Behav. Genet. in press.
S. M. Brudzynski D. Ociepa (1992) ArticleTitleUltrasonic vocalization of laboratory rats in response to handling and touch Physiol. Behav. 52 IssueID4 655–660 Occurrence Handle10.1016/0031-9384(92)90393-G Occurrence Handle1409936 Occurrence Handle1:STN:280:DyaK3s%2FivVynug%3D%3D
S. A. Brunelli M. A. Hofer (1996) ArticleTitleDevelopment of ultrasonic vocalization responses in genetically heterogeneous National Institute of Health (N:NIH) rats. II. Associations among variables and behaviors Dev. Psychobiol 29 517–528 Occurrence Handle8872425 Occurrence Handle1:STN:280:DyaK2s%2Fis1antA%3D%3D
S. A. Brunelli M. A. Hofer (2001) Selective breeding for an infantile phenotype (isolation calling): a window on developmental processes E. Blass (Eds) Handbook of behavioral neurobiology, Vol. 13, Developmental psychobiology Plenum Press New Jersey 433–482
S. A. Brunelli C. C. Keating N. A. Hamilton M. A. Hofer (1996) ArticleTitleDevelopment of ultrasonic vocalization responses in genetically heterogeneous National Institute of Health (N:NIH) rats. I. Influence of agetesting experienceand associated factors Dev. Psychobiol 29 507–516 Occurrence Handle10.1002/(SICI)1098-2302(199609)29:6<507::AID-DEV3>3.0.CO;2-Q Occurrence Handle8872424 Occurrence Handle1:STN:280:DyaK2s%2Fis1antw%3D%3D
S. A. Brunelli M. M. Myers S. L. Asekoff M. A. Hofer (2002) ArticleTitleEffects of selective breeding for infant rat ultrasonic vocalization on cardiac responses to isolation Behav. Neurosci. 116 612–623 Occurrence Handle10.1037//0735-7044.116.4.612 Occurrence Handle12148928
S. A. Brunelli H. N. Shair M. A. Hofer (1994) ArticleTitleHypothermic vocalizations of rat pups elicit and direct maternal search behavior. J. Comp. Psychol. 108 298–303 Occurrence Handle10.1037//0735-7036.108.3.298 Occurrence Handle7924260 Occurrence Handle1:STN:280:DyaK2M%2FgvVOgtQ%3D%3D
S. A. Brunelli D. D. Vinocur D. Soo-Hoo M. A. Hofer (1997) ArticleTitleFive generations of selective breeding for ultrasonic vocalization (USV) responses in N:NIH strain rats Dev. Psychobiol. 3 1255–1265
S. A. Brunelli A. Weller M. A. Hofer (2001) ArticleTitleSelective breeding for infant vocal response: a role for postnatal maternal effects? Dev. Psychobiol 38 IssueID4 221–228 Occurrence Handle10.1002/dev.1016 Occurrence Handle11319728 Occurrence Handle1:STN:280:DC%2BD3M3jtV2qsw%3D%3D
S. E. Carden M. A. Hofer (1990) ArticleTitleIndependence of benzodiazepine and opiate action in the suppression of isolation distress in rat pups Behav. Neurosci. 104 160–166 Occurrence Handle10.1037//0735-7044.104.1.160 Occurrence Handle2107826 Occurrence Handle1:STN:280:DyaK3c7psl2hug%3D%3D
S. E. Carden G. A. Barr M. A. Hofer (1991) ArticleTitleDifferential effects of specific opioid receptor agonists on rat pup isolation calls Brain Res. Dev. Brain Res. 62 17–22 Occurrence Handle10.1016/0165-3806(91)90185-L Occurrence Handle1662121 Occurrence Handle1:CAS:528:DyaK3MXmsVygu7g%3D
H. Corvoisier M. P. Moisan A. Sarrieau E. D. Hendley P. Mormede (1996) ArticleTitleBehavioral and neuroendocrine reactivity to stress in the WKHA/KY inbred rat strains: a multifactorial and genetic analysis Brain Res. 743 IssueID1–2 77–85 Occurrence Handle10.1016/S0006-8993(96)01023-2
S. V. Coutinho P. M. Plotky M. Sablad J. C. Miller H. Zhou A. I. Bayati A. McRoberts E. A. Mayer (2002) ArticleTitleNeonatal maternal separation alters stress-induced responses to viscerosomatic nociceptive stimuli in rat Am. J. Physiol. Gastrointestinal Liver Physiol. 282 G307–G316 Occurrence Handle1:CAS:528:DC%2BD38XhtFGiurc%3D
J. C. Crabbe T. J. Phillips A. Kosobud J. K. Belknap (1990) ArticleTitleEstimation of genetic correlation: Interpretation of experiments using selectively bred and inbred animals Alcoholism :Clin. Exp. Res. 14 141–151 Occurrence Handle1:STN:280:DyaK3c3nsVSqug%3D%3D
S. F. De Boer B. J. Vegt Particlevan der J. M. Koolhaas (2003) ArticleTitleIndividual variation in aggression of feral rodent strains: a standard for the genetics of aggression and violence? Behav. Genet. 33 IssueID5 485–501 Occurrence Handle10.1023/A:1025766415159 Occurrence Handle14574126
DeFries, J. C. (1981). Current perspectives on selective breeding :example and theory: In G. E. McCleam, R. A. Dietrich, and V. G. Erwin (eds), National Institute on Alcohol Abuse & Alcoholism Research Monograph 6: Development of animal models as pharmacogenetic tools. United States Department of Health and Human Services, Public Health Service: Alcohol, Drug Abuse & Mental Health Administration pp. 11-35.
R. A. Deitrich (1993) ArticleTitleSelective breeding for initial sensitivity to ethanol Behav. Genet. 23 IssueID2 153–162 Occurrence Handle8512530 Occurrence Handle1:STN:280:DyaK3s3ptVKjsQ%3D%3D
M. Durand O. Berton S. Aguerre L. Edno I. Combourieu P. Mormede F. Chaouloff (1999) ArticleTitleEffects of repeated fluoxetine on anxiety-related behaviours, central serotonergic systems, and the corticotropic axis axis in SHR and WKY rats Neuropharmacology 38 IssueID6 893–907 Occurrence Handle10.1016/S0028-3908(99)00009-X Occurrence Handle10465693 Occurrence Handle1:CAS:528:DyaK1MXjslGjt78%3D
S. A. Everson G. A. Kaplan D. E. Goldberg T. A. Lakka J. Sivenius J. T. Salonen (1999) ArticleTitleAnger expression and incident stroke: prospective evidence from the Kuopio Ischemic Heart Disease Study Stroke 30 1729–1730
S. A. Everson G. A. Kaplan J. Julkunen J. T. Salonen (1998) ArticleTitleAnger expression and incident hypertension Psychosom. Med. 60 730–735 Occurrence Handle9847033 Occurrence Handle1:STN:280:DyaK1M%2FmtFCqsg%3D%3D
A. Fernandez-Teruel R. M. Escorihuela J. A. Gray R. Aguilar L. Gil L. Gimenez-Llort A. Tobena A. Bhomra A. Nicod P. Driscoll G. E. Dawson J. Flint (2002) ArticleTitleA quantitative trait locus influencing anxiety in the laboratory rat Genome Res. 12 IssueID4 618–626 Occurrence Handle11932246 Occurrence Handle1:CAS:528:DC%2BD38XivVemt7Y%3D
G. A. Goodwin G. A. Barr (1997) ArticleTitleDevelopment of defense: role of kappa opioid receptors in the periaqueductal gray Develop. Psychobiol. 30 250
F. G. Graeff (1994) ArticleTitleNeuroanatomy and neurotransmitter regulation of defensive behaviors and related emotions in mammals Brazilian J. Med. Biol. Res. 27 811–829 Occurrence Handle1:CAS:528:DyaK2cXktVWjsro%3D
M. Graham R. Letz (1979) ArticleTitleWithin-species variation in the development of ultrasonic signaling of preweanling rats Dev. Psychobiol. 12 129–136 Occurrence Handle10.1002/dev.420120205 Occurrence Handle456751 Occurrence Handle1:STN:280:DyaE1M3hsVWqsQ%3D%3D
J. A. Gray (1972) ArticleTitleThe structure of the emotions and the limbic system Ciba Foundation Symp. 8 87–120 Occurrence Handle1:STN:280:DyaE3s7ntVemtg%3D%3D
J. A. Gray (1979) ArticleTitleEmotionality in male and female rodents: a reply to Archer Brit. J. Psychol. 70 IssueID3 425–440 Occurrence Handle486879 Occurrence Handle1:STN:280:DyaL3c%2FitFOmuw%3D%3D
M. E. Hahn J. K. Hewitt M. Adams T. Tully (1987) ArticleTitleGenetic influences on ultrasonic vocalizations in young mice Behav. Genet. 17 IssueID2 155–166 Occurrence Handle3606538 Occurrence Handle1:STN:280:DyaL2s3ntVGmtA%3D%3D
M. E. Hahn J. K. Hewitt N. Schanz L. Weinreb A. Henry (1997) ArticleTitleGenetic and developmental influences on infant mouse ultrasonic calling. I. A diallel analysis of the calls of 3-day-olds Behav. Genet. 27 IssueID2 133–143 Occurrence Handle10.1023/A:1025637408900 Occurrence Handle9145552 Occurrence Handle1:STN:280:DyaK2s3ptV2htA%3D%3D
Hahn, M. E., and Lavooy, M. J. A review of the methods of studies on infant ultrasound production and maternal retrieval in small rodents. Behav. Genet. in press.
C. Hansen K. Spuhler (1984) ArticleTitleDevelopment of the National Institutes of Health genetically heterogeneous rat stock Alcoholism: Clin. Exp. Res. 8 477–479 Occurrence Handle1:STN:280:DyaL2M%2FntVWltg%3D%3D
A. T. Harvey M. B. Hennessy (1995) ArticleTitleCorticotropin-releasing factor modulation of the ultrasonic rate of isolated pups Dev. Brain Res. 87 125–134 Occurrence Handle10.1016/0165-3806(95)00064-K Occurrence Handle1:CAS:528:DyaK2MXmvF2nur4%3D
K. W. Heaton L. J. O’Donnell F. E. Braddon R. A. Mountford A. O. Hughes P. J. Cripps (1992) ArticleTitleSymptoms of irritable bowel syndrome in a British urban community: consulters and nonconsulters. Gastroenterology 102 IssueID6 1962–1967 Occurrence Handle1587415 Occurrence Handle1:STN:280:DyaK383mslaqtQ%3D%3D
N. D. Henderson (1997) ArticleTitleSpurious associations in unreplicated selected lines Behav. Genet. 27 IssueID2 145–154 Occurrence Handle10.1023/A:1025689425738 Occurrence Handle9145553 Occurrence Handle1:STN:280:DyaK2s3ptV2htQ%3D%3D
N. D. Henderson M. G. Turri J. C. DeFries J. Flint (2004) ArticleTitleQTL analysis of multiple behavioral measures of anxiety in mice Behav. Genet. 34 267–293 Occurrence Handle10.1023/B:BEGE.0000017872.25069.44 Occurrence Handle14990867
M. B. Hennessy J. Weinberg (1990) ArticleTitleAdrenocortical activity during conditions of brief maternal separation in preweaning rats Behav. Neural Biol. 54 42–55 Occurrence Handle10.1016/0163-1047(90)91231-Y Occurrence Handle2378605 Occurrence Handle1:CAS:528:DyaK3cXlt1Kks7Y%3D
D. R. Hirshfeld J. F. Rosenbaum J. Biederman E. A. Bolduc S. V. Faraone N. Snidman J. S. Reznick J. Kagan (1992) ArticleTitleStable behavioral inhibition and its association with anxiety disorder. J. Am. Acad. Child Adoles. Psychiat. 31 IssueID1 103–111 Occurrence Handle1:STN:280:DyaK387msFKrtA%3D%3D Occurrence Handle10.1097/00004583-199201000-00016
M. A. Hofer (1984) ArticleTitleEarly stages in the organization of cardiovascular control Proceedings of the Society for Experimental Biology and Medicine 175 147–157 Occurrence Handle6694973 Occurrence Handle1:STN:280:DyaL2c7hvFGruw%3D%3D
M. A. Hofer (1994) ArticleTitleEarly relationships as regulators of infant physiology and behavior Acta PaeditricaSupplement 397 735–738
M. A. Hofer (1996) ArticleTitleMultiple regulators of ultrasonic vocalization in the infant rat Psychoneuroendocrinology 21 IssueID2 203–217 Occurrence Handle10.1016/0306-4530(95)00042-9 Occurrence Handle8774063 Occurrence Handle1:STN:280:DyaK28zntVWhtg%3D%3D
M. A. Hofer M. F. Reiser (1969) ArticleTitleThe development of cardiac rate regulation in preweanling rats Psychosom. Med. 31 372–388 Occurrence Handle5350296 Occurrence Handle1:CAS:528:DyaE3cXivFCktg%3D%3D
T. R. Insel J. L. Hill (1987) ArticleTitleInfant separation distress in genetically fearful rats Biol. Psychiatr. 22 783–786 Occurrence Handle10.1016/0006-3223(87)90214-9
T. R. Insel J. T. Winslow (1991) Rat pup ultrasonic vocalizations :an ethologically relevant behavior responsive to anxiolytics Birkhaauser Verlag Basel 15–36
M. P. Joyce S. E. Carden (1999) ArticleTitleThe effects of 8-OH-DPAT and (+/-)-pindolol on isolation-induced ultrasonic vocalizations in 3-, 10-, and 14-day-old rats Dev. Psychobiol. 34 109–117 Occurrence Handle10086229 Occurrence Handle1:CAS:528:DyaK1MXitVersr4%3D
J. Kagan (1987) ArticleTitleTemperament and the reactions to unfamiliarity Child Dev. 68 139–143
J. Kagan J. S. Reznick J. Gibbons (1989) ArticleTitleInhibited and uninhibited types of children Child Dev. 60 838–845 Occurrence Handle2758880 Occurrence Handle1:STN:280:DyaL1MzjslOrtw%3D%3D
J. Kagan J. S. Reznick N. Snidman (1987) ArticleTitleThe physiology and psychology of behavioral inhibition in children Child Dev. 58 1459–1473 Occurrence Handle3691195 Occurrence Handle1:STN:280:DyaL1c%2FotFyhtw%3D%3D
J. Kagan N. Snidman (1991) ArticleTitleTemperamental factors in human development Am. Psychol. 46 856–862 Occurrence Handle10.1037//0003-066X.46.8.856 Occurrence Handle1928938 Occurrence Handle1:STN:280:DyaK38%2FislWgsA%3D%3D
J. Kagan N. Snidman (1999) ArticleTitleEarly childhood predictors of adult anxiety disorders Biol. Psychiat. 46 IssueID11 1536–1541 Occurrence Handle10.1016/S0006-3223(99)00137-7 Occurrence Handle10599481 Occurrence Handle1:STN:280:DC%2BD3c%2FmslGrug%3D%3D
J. H. Kehne T. C. McCloskey B. M. Baron E. M. Chi B. L. Harrison J. P. Whitten M. G. Palfreyman (1991) ArticleTitleNMDA receptor complex antagonists have potential anxiolytic effects as measured with separation-induced ultrasonic vocalizations Eur. J. Pharmacol. 193 283–292 Occurrence Handle10.1016/0014-2999(91)90141-C Occurrence Handle1675993 Occurrence Handle1:CAS:528:DyaK3MXhvF2mtr0%3D
J. M. Koolhaas S. M. Korte S. F. De Boer B. J. Van Der Vegt C. G. Van Reenen H. Hopster I. C. De Jong M. A. Ruis H. J. Blokhuis (1999) ArticleTitleCoping styles in animals :current status in behavior and stress-physiology Neurosci. Biobehav. Rev. 23 925–935 Occurrence Handle10.1016/S0149-7634(99)00026-3 Occurrence Handle10580307 Occurrence Handle1:STN:280:DC%2BD3c%2Fks1amsA%3D%3D
D. J. Laurie W. Wisden P. H. Seeburg (1992) ArticleTitleThe distribution of thirteen GABAA receptor subunit mRNAs in the rat brain III Embryonic and postnatal development J. Neurosci. 12 4151–4172 Occurrence Handle1331359 Occurrence Handle1:CAS:528:DyaK3sXhs1Okuw%3D%3D
R. B. Lydiard S. Greenwald M. M. Weissman J. Johnson D. A. Drossman J. C. Ballenger (1994) ArticleTitlePanic disorder and gastrointestinal symptoms: findings from the NIMH Epidemiologic Catchment Area project Am. J. Psychiatr. 151 64–70 Occurrence Handle8267136 Occurrence Handle1:STN:280:DyaK2c%2FptFGisQ%3D%3D
S. E. Maier P. Vandenhoff D. P. Crowne (1988) ArticleTitleMultivariate analysis of putative measures of activity, exploration, emotionality, and spatial behavior J. Compar. Psychol. 102 378–387 Occurrence Handle10.1037//0735-7036.102.4.378 Occurrence Handle1:STN:280:DyaL1M7gs1Kltw%3D%3D
M. Million L. Wang V. Martinez Y. Tache (2000) ArticleTitleDifferential Fos expression in the paraventricular nucleus of the hypothalamus, sacral parasympathetic nucleus and colonic motor reponse to water avoidance stress in Fischer and Lewis rats Brain Res. 877 345–353 Occurrence Handle10.1016/S0006-8993(00)02719-0 Occurrence Handle10986349 Occurrence Handle1:CAS:528:DC%2BD3cXmtlGrsL0%3D
C. Monk W. P. Fifer M. M. Myers R. P. Sloan L. Trien A. Hurtado (2000) ArticleTitleMaternal stress responses and anxiety during pregnancy: effects on fetal heart rate Dev. Psychobiol. 36 67–77 Occurrence Handle10.1002/(SICI)1098-2302(200001)36:1<67::AID-DEV7>3.3.CO;2-3 Occurrence Handle10607362 Occurrence Handle1:STN:280:DC%2BD3c%2FnsVyrsQ%3D%3D
P. Mormede H. Courvoisier A. Ramos N. Marissal-Arvy O. Ousova C. Desautes M. Duclos F. Chaouloff M. P. Moisan (2002) ArticleTitleMolecular genetic approaches to investigate individual variations in behavioral and neuroendocrine stress responses Psychoneuroendocrinology 27 IssueID5 563–583 Occurrence Handle10.1016/S0306-4530(01)00093-2 Occurrence Handle11965355 Occurrence Handle1:CAS:528:DC%2BD38XivVSnsbw%3D
M. M. Myers (1992) ArticleTitleBehavioral and cardiovascular traits. Broken links and new associations. Annu. New York Acad. Sci. 662 84–101 Occurrence Handle1:STN:280:DyaK3s%2FovFOksg%3D%3D
E. Noirot (1972) ArticleTitleUltrasounds and maternal behavior in small rodents Dev. Psychobiol. 5 371–387 Occurrence Handle10.1002/dev.420050410 Occurrence Handle4609822 Occurrence Handle1:STN:280:DyaE2M%2FjvFCkuw%3D%3D
S. C. Nuding I. Nadelhaft (1998) ArticleTitleBilateral projections of the pontine micturition center to the sacral parasympathetic nucleus in the rat Brain Res. 785 185–194 Occurrence Handle10.1016/S0006-8993(97)01347-4 Occurrence Handle9518605 Occurrence Handle1:CAS:528:DyaK1cXhvVSjt7s%3D
B. Olivier E. Molewijk R. van Oorschot J. van der Heyden E. Ronken J. Mos (1998a) ArticleTitleRat pup ultrasonic vocalization: effects of benzodiazepine receptor ligands Eur. J. Pharmacol. 358 117–128 Occurrence Handle10.1016/S0014-2999(98)00603-7 Occurrence Handle1:CAS:528:DyaK1cXmt1emtr0%3D
B. Olivier H. E. Molewijk J. A. van der Heyden R. van Oorschot E. Ronken J. Mos K. A. Miczek (1998b) ArticleTitleUltrasonic vocalizations in rat pups: effects of serotonergic ligands Neurosci. Biobehav. Rev. 23 215–227 Occurrence Handle10.1016/S0149-7634(98)00022-0 Occurrence Handle1:CAS:528:DyaK1MXlsF2lsg%3D%3D
D. H. Overstreet (2002) ArticleTitleBehavioral characteristics of rat lines selected for differential hypothermic responses to cholinergic or serotonergic agonists Behav. Genet. 32 IssueID5 335–348 Occurrence Handle10.1023/A:1020262205227 Occurrence Handle12405515
D.S Pine G. A. Wasserman L. Miller J. D. Coplan E. Bagiella P. Kovelenku M. M. Myers R. P. Sloan (1998) ArticleTitleHeart period variability and psychopathology in urban boys at risk for delinquency Psychophysiology 35 IssueID5 521–529 Occurrence Handle10.1017/S0048577298970846 Occurrence Handle9715096 Occurrence Handle1:STN:280:DyaK1czotVyhug%3D%3D
R. Plomin J. C. DeFries G. E. McClearn (1991) Behavioral genetics :a primer W. H. Freeman & Co New York
A. Ramos O. Berton P. Mormede F. Chaouloff (1997) ArticleTitleA multiple-test study of anxiety-related behaviors in six inbred rat strains Behav. Brain Res. 85 IssueID1 57–69 Occurrence Handle10.1016/S0166-4328(96)00164-7 Occurrence Handle9095342 Occurrence Handle1:STN:280:DyaK2s3kvFCmtA%3D%3D
A. Ramos E. C. Correia G. S. Izidio G. R. Bruske (2003) ArticleTitleGenetic selection of two new rat lines displaying different levels of anxiety-related behaviors Behav. Genet. 33 IssueID6 657–668 Occurrence Handle10.1023/A:1026131130686 Occurrence Handle14574121
A. Ramos Y. Mellerin P. Mormede F. Chaouloff (1998) ArticleTitleA genetic and multifactorial analysis of anxiety-related behaviours in Lewis and SHR intercrosses Behav. Brain Res. 96 IssueID12 195–205 Occurrence Handle10.1016/S0166-4328(98)00023-0 Occurrence Handle9821556 Occurrence Handle1:STN:280:DyaK1M%2FjvV2qtQ%3D%3D
A. Ramos P. Mormède (1998) ArticleTitleStress and emotionality: A multidimensional and genetic approach Neurosci. Biobehav. Rev. 22 IssueID1 33–57 Occurrence Handle10.1016/S0149-7634(97)00001-8 Occurrence Handle9491939 Occurrence Handle1:STN:280:DyaK1c7ltV2jsQ%3D%3D
A. Ramos M. P. Moisan F. Chaouloff C. Mormede P. Mormede (1999) ArticleTitleIndentification of female-specific QTLs affecting an emotionally-related behavior in rats. Mol. Psychiat. 4 IssueID5 453–462 Occurrence Handle10.1038/sj.mp.4000546 Occurrence Handle1:CAS:528:DC%2BD3cXlvVWltbk%3D
Rojowski, H. M., Brunelli, S. A., Shair, H. N., and Hofer, M. A. (1999). Adult plus maze performance in rats selectively bred for infant ultrasonic vocalizations (USV) rates Abstract International Society for Developmental Psychobiology
Rojowski, H. M., Weller. A., Hofer, M. A., and Brunelli, S.A. (2000). Maternal behavior in rats selectively bred for infant ultrasonic vocalization (USV). Abstract International Society for Developmental Psychobiology.
J. F. Rosenbaum J. Biederman D. R. Hirshfeld E. A. Bolduc S. V. Faraone J. Kagan N. Snidman J. S. Reznick (1991) ArticleTitleFurther evidence of an association between behavioral inhibition and anxiety disorders: results from a family study of children from a non-clinical sample J. Psychiat. Res. 25 49–65 Occurrence Handle10.1016/0022-3956(91)90015-3 Occurrence Handle2027095 Occurrence Handle1:STN:280:DyaK3M3isF2itw%3D%3D
J. F. Rosenbaum J. Biederman D. R. Hirschfeld-Becker J. Kagan J. Snidman D. Friedman A. Nineberg D. J. Gallery S. V. Faraone (2000) ArticleTitleA controlled study of behavioral inhibition in children of parents with panic disorder and depression Am. J. Psychiatr. 157 2002–2010 Occurrence Handle10.1176/appi.ajp.157.12.2002 Occurrence Handle11097967 Occurrence Handle1:STN:280:DC%2BD3M%2Fps1OrtA%3D%3D
P. L. Roubertoux (2001) ArticleTitleLetter to the Editor:Chronicle for an orphan trait :Comment on HoferShairMasmela& Brunelli“Developmental effects of selective breeding fo an infantile trait: The rat pup ultrasonic isolation call” Dev. Psychobiol. 39 251–254 Occurrence Handle10.1002/dev.1002 Occurrence Handle11745320 Occurrence Handle1:STN:280:DC%2BD3Mnps1eqsA%3D%3D
P.L. Roubertoux B. Martin I. LeRoy J. Beau C. Marchaland F. Perez-Diaz C. Cohen-Salmon M. Carlier (1996) ArticleTitleVocalizations in newborn mice: Genetic analysis Behav. Genet. 26 IssueID4 427–437 Occurrence Handle8771903 Occurrence Handle1:STN:280:DyaK28zmslOruw%3D%3D
C. E. Schwartz N. Snidman J. Kagan (1999) ArticleTitleAdolescent social anxiety as an outcome of inhibited temperament in childhood J. Am. Acad. Child Adol. Psychiatr. 38 IssueID8 1008–1015 Occurrence Handle10.1097/00004583-199908000-00017 Occurrence Handle1:STN:280:DyaK1MzmtlegtQ%3D%3D
C. E. Schwartz C. I. Wright L. M. Shin J. Kagan S. L. Rauch (2003) ArticleTitleInhibited and uninhibited infants “grown up”: Adult amygdalar response to novelty Science 300 1952–1953 Occurrence Handle10.1126/science.1083703 Occurrence Handle12817151 Occurrence Handle1:CAS:528:DC%2BD3sXks1Kmu7k%3D
Shair, H. N., Brunelli, S. A., Velazquez, Z., and Hofer, M.A. (2000). Adult behavioral tests of rats selectively bred for infantile ultrasonic vocalization. Abstract International Society for Developmental Psychobiology.
R. P. Sloan P. A. Shapiro J. T. Bigger E. Bagiella R. C. Steimnan J. M. Gorman (1994) ArticleTitleCardiac autonomic control and hostility in healthy subjects Am. J. Cardiol. 74 298–300 Occurrence Handle10.1016/0002-9149(94)90382-4 Occurrence Handle8037145 Occurrence Handle1:STN:280:DyaK2czhtFagug%3D%3D
R. P. Sloan P. A. Shapiro E. Bagiella M. M. Myers J. M. Gorman (1999) ArticleTitleCardiac autonomic control buffers blood pressure variability responses to challenge: a psychophysiological model of coronary artery disease Psychosom. Med. 61 58–68 Occurrence Handle10024068 Occurrence Handle1:STN:280:DyaK1M7ks1KksQ%3D%3D
D. P. Snustad M. J. Simmons J. B. Jenkins (1997) Principles of genetics John Wiley & Sons, Inc. New York, NY
R. Stam G. Croiset L. M. Akkermans V. M. Wiegant (1997) ArticleTitleBehavioral and intestinal responses to novelty in rats selected for diverging reactivity in the open field test Behav. Brain Res. 88 IssueID2 231–238 Occurrence Handle10.1016/S0166-4328(97)00046-6 Occurrence Handle9404632 Occurrence Handle1:STN:280:DyaK1c%2FmvVCnsQ%3D%3D
R. Stam G. Croiset A. W. Bruijnzeel T. J. Visser L. M. Akkermans V. M. Wiegant (1999) ArticleTitleSex differences in long-term stress-induced colonic, behavioral and hormonal disturbances Life Sci. 65 IssueID26 2837–2839 Occurrence Handle10.1016/S0024-3205(99)00553-6 Occurrence Handle10622273 Occurrence Handle1:CAS:528:DyaK1MXns1elt78%3D
Thornton, L. M., Hahn, M. E., and Schanz, N. Genetic and developmental influences on infant mouse ultrasonic calling III Patterns of inheritance in the calls of mice 3–9 days of age. Behav. Genet., in press
R. J. Valentino M. E. Page P. H. Luppi Y. Zhu E. Van Bockstaele G. Aston-Jones (1994) ArticleTitleEvidence of widespread afferents to Barrington’s nucleus, a brainstern rich in corticotropin-releasing hormone Neuroscience 62 IssueID1 125–143 Occurrence Handle10.1016/0306-4522(94)90320-4 Occurrence Handle7816195 Occurrence Handle1:STN:280:DyaK2M7hsFyltA%3D%3D
V. Warner M. M. Weissman L. Mufson P. J. Wickramaratne (1999) ArticleTitleGrandparents, parents, and grandchildren at high risk for depression: a three-generation study J. Acad. Child Adol. Psychiatr. 38 IssueID3 289–296 Occurrence Handle10.1097/00004583-199903000-00017 Occurrence Handle1:STN:280:DyaK1M7oslKmtg%3D%3D
M. M. Weissman R. C. Bland G. J. Canino C. Faravelli S. Greenwald H. G. Hwu P. R. Joyce E. G. Karam C. K. Lee J. Lellouch J. P. Lepine S. C. Newman M. Rubio-Stipee J. E. Wells P. J. Wickramaratne H. Wittchen E. K. Yeh (1996) ArticleTitleCross-national epidemiology of major depression and bipolar disorder JAAM 276 IssueID4 293–299 Occurrence Handle10.1001/jama.276.4.293 Occurrence Handle1:STN:280:DyaK283os1Wnsw%3D%3D
G. D. Whitney J. Nyby J. R. Cable G. A. Dizinno (1978) ArticleTitleGenetic influences on 70 kHz ultrasound production of mice (Mus musculus) Behav. Genet. 8 IssueID6 574–578
P. J. G. S. Wickramaratne M. M. Weissman (2000) ArticleTitlePsychiatric disorders in the relatives of probands with prepubertal-onset or adolescent-onset major depression J. Am. Acad. Child Adol. Psychiatr. 39 IssueID11 1396–1405 Occurrence Handle10.1097/00004583-200011000-00014 Occurrence Handle1:STN:280:DC%2BD3crhtFKnsg%3D%3D
J. T. Winslow T. R. Insel R. Trullas P. Skolnick (1990) ArticleTitleRat pup isolation calls are reduced by functional antagonists of the NMDA receptor complex Eur. J. Pharmacol. 190 11–21 Occurrence Handle10.1016/0014-2999(90)94107-9 Occurrence Handle1963846 Occurrence Handle1:CAS:528:DyaK3MXjs1CmtA%3D%3D
V. K. Yeragani (1995) ArticleTitleHeart rate and blood pressure variability :Implications for psychiatric research Neuropsychobiology 32 182–191 Occurrence Handle10.1159/000119234 Occurrence Handle8587700 Occurrence Handle1:STN:280:DyaK287lvF2htQ%3D%3D
V. K. R. K. A. Yeragani R. Pohl V. C. Jampala R. Balon (2001) ArticleTitleHeart rate and QT variability in children with anxiety disorders: a preliminary report Depress. Anxiety 13 72–77 Occurrence Handle10.1002/da.1019 Occurrence Handle11301923 Occurrence Handle1:STN:280:DC%2BD3Mris1eksA%3D%3D
T. Yoshikawa A. Watanabe Y. Ishitsuka A. Nakaya N. Nakatani (2002) ArticleTitleIdentification of multiple genetic loci linked to the propensity for “behavioral despair” in mice Genome Res. 12 357–366 Occurrence Handle10.1101/gr.222602 Occurrence Handle11875023 Occurrence Handle1:CAS:528:DC%2BD38XitFSlt7k%3D
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Brunelli, S.A. Selective Breeding for an Infant Phenotype: Rat Pup Ultrasonic Vocalization (USV). Behav Genet 35, 53–65 (2005). https://doi.org/10.1007/s10519-004-0855-6
Issue Date:
DOI: https://doi.org/10.1007/s10519-004-0855-6