Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2019 | 79 | 1 |
Tytuł artykułu

Distinct classes of low frequency ultrasonic vocalizations in rats during sexual interactions relate to different emotional states

Warianty tytułu
Języki publikacji
This study examined low-frequency ultrasonic vocalizations (lUSVs) in rats during two types of sexual interactions: postejaculatory interval (PEI) and barrier – noncontact (NC) test. We report distinct classes of IUSVs that can be assigned to different emotional states; relaxation vs. frustration. Totally flat, 22-kHz calls (Class A), were observed during the relaxation state following ejaculation; characterized by immobilization or grooming during the PEI. On the other hand, twothree component IUSVs (Class B) that start at a higher frequency (45-kHz: flat, upward or short signal) and then shift to 35-23kHz (mostly to 2823-kHz), correspond as we assume, to arousal and frustration – active states associated with sniffing a hole or exploration during the NC test. We suggest that momentary, abrupt decreases of arousal during the frustration state correspond to Class B IUSVs. The detailed spectral analysis of the high-frequency component of twocomponent IUSVs is crucial for establishing the relationship between such IUSVs and the corresponding behavior and emotional states. Our studies indicate that while the twocomponent Class B 22-kHz IUSVs may relate to the frustration state, a single component, flat, Class A IUSV relates to the relaxation state. The results of these studies support a notion that rats emit distinct vocalization patterns, reflecting their emotional states.
Słowa kluczowe
Opis fizyczny
  • Laboratory of Centre for Preclinical Research, Department of Experimental and Clinical Physiology, Medical University of Warsaw, Poland
  • Laboratory of Centre for Preclinical Research, Department of Experimental and Clinical Physiology, Medical University of Warsaw, Poland
  • Department for Experimental Medicine, Medical University of Silesia, Katowice, Poland
  • Laboratory of Centre for Preclinical Research, Department of Experimental and Clinical Physiology, Medical University of Warsaw, Poland
  • Laboratory of Centre for Preclinical Research, Department of Experimental and Clinical Physiology, Medical University of Warsaw, Poland
  • Department of Psychiatry, Harvard Medical School, Boston MA, USA
  • Ågmo A, Snoeren EM (2015) Silent or vocalizing rats copulate in a similar manner. PLoS One 10: e0144164.
  • Amsel A (1958) The role of frustrative nonreward in noncontinuous reward situations. Psychol Bull 55: 102–119.
  • Amsel A (1992) Frustration theorymany years later. Psychol Bull 112: 396–399.
  • Arriaga G, Jarvis ED (2013) Mouse vocal communication system: are ultrasounds learned or innate? Brain Lang 124: 96–116.
  • Asaba A, Hattori T, Mogi K, Kikusui T (2014) Sexual attractiveness of male chemicals and vocalizations in mice. Front Neurosci 8: 231.Bang SJ, Allen TA, Jones LK, Boguszewski P, Brown TH (2008) Asymmetrical stimulus generalization following differential fear conditioning. Neurobiol Learn Mem 90: 200–216.
  • Barfield RJ, Geyer LA (1972) Sexual behavior: ultrasonic postejaculatory song of the male rat. Science 176: 1349–1350.
  • Barfield RJ, Geyer LA (1975) The ultrasonic postejaculatory vocalization and the postejaculatory refractory period of the male rat. J Comp Physiol Psychol 88: 723–734.
  • Beck J, Bialy M, Kostowski W (2002) Effects of D(1) receptor agonist SKF 38393 on male rat sexual behavior and postcopulatory departure in the goal compartmentrunway paradigm. Physiol Behav 76: 91–97.
  • Bell RW (1974) Ultrasounds in small rodents: arousalproduced and arousalproducing. Dev Psychobiol 7: 39–42.
  • Bialy M, BogackiRychlik W, Kasarello K, Nikolaev E, SajdelSulkowska EM (2016) Modulation of 22khz postejaculatory vocalizations by conditioning to new place: Evidence for expression of a positive emotional state. Behav Neurosci 130: 415–421.
  • Bialy M, BogackiRychlik W, CudnochJedrzejewska A (2018) The low frequency ultrasonic vocalizations (22kHz) as the effect of abrupt decrease of arousal in rats: Evidence from postejaculatory vocalizations during exposition to 5HT1A receptor agonist. 5th Seminar on Behavioral Methods Krakow, 27–27 September, p 2.
  • Bialy M, Kalata U, NikolaevDiak A, Nikolaev E (2010) D1 receptors involved in the acquisition of sexual experience in male rats. Behav Brain Res 206: 166–176.
  • Bialy M, NikolaevDiak A, Kalata U, Nikolaev E (2011) Blockade of androgen receptor in the medial amygdala inhibits noncontact erections in male rats. Physiol Behav 103: 295–301.
  • Bialy M, Rydz M, Kaczmarek L (2000) Precontact 50kHz vocalizations in male rats during acquisition of sexual experience. Behav Neurosci 114: 983–990.
  • Bialy M, Sachs BD (2002) Androgen implants in medial amygdala briefly maintain noncontact erection in castrated male rats. Horm Behav 42: 345–355.
  • Bialy M, Strefnel M, NikolaevDiak A, Socha A, Nikolaev E, Boguszewski P (2014) Sexual performance and precontact 50kHz ultrasonic vocalizations in WAG/Rij rats: Effects of opioid receptor treatment. Epilepsy Behav 39: 66–72.
  • Blanchard RJ, Blanchard DC, Agullana R, Weiss SM (1991) Twentytwo kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems. Physiol Behav 50: 967–972.
  • Blumberg MS, Alberts JR (1991) On the significance of similarities between ultrasonic vocalizations of infant and adult rats. Neurosci Biobehav Rev 15: 383–390.
  • Blumberg MS, Moltz H (1987) Hypothalamic temperature and the 22 kHz vocalization of the male rat. Physiol Behav 40: 637–640.
  • Brown RE (1979) The 22kHz preejaculatory vocalizations of the male rat. Physiol Behav 22: 483–489.
  • Brudzynski SM (2007) Ultrasonic calls of rats as indicator variables of negative or positive states: acetylcholinedopamine interaction and acoustic coding. Behav Brain Res 182: 261–273.
  • Brudzynski SM (2015) Pharmacology of ultrasonic vocalizations in adult rats: Significance, call classification and neural substrate. Curr Neuropharmacol 13: 180–192.
  • Brudzynski SM, Bihari F, Ociepa D, Fu XW (1993) Analysis of 22 kHz ultrasonic vocalization in laboratory rats: long and short calls. Physiol Behav 54: 215–221.
  • Burgdorf J, Kroes RA, Moskal JR, Pfaus JG, Brudzynski SM, Panksepp J (2008) Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: Behavioral concomitants, relationship to reward, and selfadministration of playback. J Comp Psychol 122: 357–367.
  • Burgdorf J, Panksepp J, Moskal JR (2018) Rat 22kHz ultrasonic vocalizations as a measure of emotional set point during social interactions. In: Handbook of Behavioral Neuroscience (Brudzynski SM, Ed.). Elsevier B.V., Vol. 25, p. 261–265. Burke CJ, Kisko TM, Pellis SM, Euston DR (2017) Avoiding escalation from play to aggression in adult male rats: The role of ultrasonic calls. Behav Processes 144: 72–81.
  • Cagiano R, Barfield RJ, White NR, Pleim ET, Cuomo V (1989) Mediation of rat postejaculatory 22 kHz ultrasonic vocalization by dopamine D2 receptors. Pharmacol Biochem Behav 34: 53–58.
  • Calvino B, Besson JM, Boehrer A, Depaulis A (1996) Ultrasonic vocalization (22–28 kHz) in a model of chronic pain, the arthritic rat: effects of analgesic drugs. Neuroreport 7: 581–584.
  • Dudley RT, Papini MR (1997) Amsel’s frustration effect: a pavlovian replication with control for frequency and distribution of rewards. Physiol Behav 61: 627–629.
  • Engelhardt KA, Fuchs E, Schwarting RKW, Wöhr M (2017) Effects of amphetamine on prosocial ultrasonic communication in juvenile rats: Implications for mania models. Eur Neuropsychopharmacol 27: 261–273.
  • Filipkowski RK, Polowy R, Malz M, Gawrys O, Olszynski KH (2017) Ultrasonic and cardiovascular responses to ultrasonic sounds and vocalizations. Acta Neurobiol Exp 77: CXXIVCXXV.
  • Freidin E, Mustaca AE (2004) Frustration and sexual behavior in male rats. Learn Behav 32: 311–320.
  • Geyer LA, Barfield RJ, McIntosh TK (1978) Influence on gonadal hormones and sexual behavior on ultrasonic vocalization in rats: II. Treatment of males, J Comp Physiol Psychol 92: 447–456.
  • Hernandez C, Sabin M, Riede T (2017) Rats concatenate 22 kHz and 50 kHz calls into a single utterance. J Exp Biol 220: 814–821.
  • Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS Biol 3: e386.
  • Hull EM, RodríguezManzo, G. (2017) Male Sexual Behavior. In: Hormones, Brain, and Behavior (Pfaff DW and Joëls M, editorsinchief). Oxford Academic Press; 3rd edition, Vol. 1, p. 1–57.
  • Inagaki H, Mori Y (2015) The emission of stressinduced 22kHz calls in female rats is independent of testosterone levels. Horm Behav 69: 116–118.
  • Jelen P, Soltysik S, Zagrodzka J (2003) 22kHz ultrasonic vocalization in rats as an index of anxiety but not fear: behavioral and pharmacological modulation of affective state. Behav Brain Res 141: 63–72.
  • Kondo Y, Sachs BD (2002) Disparate effects of small medial amygdala lesions on noncontact erection, copulation, and partner preference. Physiol Behav 76: 443–447.
  • Lorrain DS, Riolo JV, Matuszewich L, Hull EM (1999) Lateral hypothalamic serotonin inhibits nucleus accumbens dopamine: implications for sexual satiety. J Neurosci 19: 7648–7652.
  • Mos J, Van Logten J, Bloetjes K, Olivier B (1991) The effects of idazoxan and 8OHDPAT on sexual behaviour and associated ultrasonic vocalizations in the rat. Neurosci Biobehav Rev 15: 505–515.
  • Naito H, Okumura T, Inoue M, Suzuki Y (2006) Ultrasonic vocalization response elicited in adjuvantinduced arthritic rats as a useful method for evaluating analgesic drugs. Exp Anim 55: 125–129.
  • Reno JM, Thakore N, Gonzales R, Schallert T, Bell RL, Maddox WT, Duvauchelle CL (2015) Alcoholpreferring P rats emit spontaneous 2228 kHz ultrasonic vocalizations that are altered by acute and chronic alcohol experience. Alcohol Clin Exp Res 39: 843–852.
  • RodriguezManzo G, FernándezGuasti (1994) Reversal of sexual exhaustion by serotonergic and noradrenergic agents. Behav Brain Res 62: 127–134.
  • Sachs BD (1997) Erection evoked in male rats by airborne scent from estrous females. Physiol Behav 62: 921–924.
  • Sachs BD (2000) Contextual approaches to the physiology and classification of erectile function, erectile dysfunction, and sexual arousal. Neurosci Biobehav Rev 24: 541–560.
  • Sachs BD, Akasofu K, Citron JH, Daniels SB, Natoli JH (1994) Noncontact stimulation from estrous females evokes penile erection in rats. Physiol Behav 55: 1073–1079.
  • Sachs BD, Barfield RJ (1976) Functional analysis of masculine copulatory behavior in the rat. Adv Study Behav 7: 91–154.Sachs BD, Bialy M (2000) Female presence during postejaculatory interval facilitates penile erection and 22kHz vocalization in male rats. Behav Neurosci 114: 1203–1208.
  • Sales GD, Pye JD (1974) Ultrasonic communication by animals. Chapman and Hall. London, England,–94–011–6901–1.
  • Snoeren EM, Agmo A (2013) Female ultrasonic vocalizations have no incentive value for male rats. Behav Neurosci 127: 439–450.
  • Takeuchi H, Kawashima S (1986) Ultrasonic vocalizations and aggressive behavior in male rats. Physiol Behav 38: 545–550.
  • Thakore N, Reno JM, Gonzales RA, Schallert T, Bell RL, Maddox WT, Duvauchelle CL (2016) Alcohol enhances unprovoked 22–28 kHz USVs and suppresses USV mean frequency in High Alcohol Drinking (HAD1) male rats. Behav Brain Res 302: 228–236.
  • Thomas DA, Howard SB, Barfield RJ (1982) Maleproduced postejaculatory 22kHz vocalizations and the mating behavior of estrous female rats. Behav Neural Biol 36: 403–410.
  • Thomas DA, Barfield RJ (1985) Ultrasonic vocalization of the female rat (Rattus norvegicus) during mating. Animal Behav. 33: 720–725.
  • Van der Poel AM, Miczek KA (1991) Long ultrasonic calls in male rats following mating, defeat and aversive stimulation: Frequency modulation and bout structure. Behaviour 119: 127–142. Vivian JA, Miczek KA (1993a) Morphine attenuates ultrasonic vocalization during agonistic encounters in adult male rats. Psychopharmacol 111: 367–375.
  • Vivian JA, Miczek KA (1993b) Diazepam and gepirone selectively attenuate either 20–32 or 32–64 kHz ultrasonic vocalizations during aggressive encounters. Psychopharmacol 112: 66–73.
  • Vivian JA, Miczek KA (1999) Interactions between social stress and morphine in the periaqueductal gray: effects on affective vocal and reflexive pain responses in rats. Psychopharmacol 146: 153–161.
  • White NR, Barfield RJ (1987) Role of the ultrasonic vocalization of the female rat (Rattus norvegicus) in sexual behavior. J Comp Psychol 101: 73–81.
  • Wöhr M (2018) Ultrasonic communication in rats: appetitive 50kHz ultrasonic vocalizations as social contact calls. Behav Ecol Sociobiol 72: 14.
  • Wöhr M, Schwarting RK (2007) Ultrasonic communication in rats: can playback of 50kHz calls induce approach behavior? PLoS One 2: e1365.
  • Wöhr M, Schwarting RK (2009) Ultrasonic communication in rats: effects of morphine and naloxone on vocal and behavioral responses to playback of 50kHz vocalizations. Pharmacol Biochem Behav 94: 285–295.
Typ dokumentu
Identyfikator YADDA
JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.