Effects of maternal deprivation and the duration of reunion time on rat pup ultrasonic vocalization responses to isolation: Possible implications for human infant studies

Developmental Psychobiology

Volumn 57, Issue 1, 2015, Pages 63-72

  Shair, Harry N ^a,b   Rupert, Deborah D ^b   Rosko, Lauren M ^b   Hofer, Myron A ^a,b   Myers, Michael M ^a,b   Welch, Martha G ^b  

^a NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^b Columbia University College of Physicians and Surgeons ^*  (United States)

Author keywords

Contact quieting; Isolation; Maternal odor; Maternal potentiation; Maternal reunion; Maternal separation; Neonatal intensive care; Olfaction; Ultrasonic vocalization

Indexed keywords

RATTUS;

ANIMAL; FEMALE; LONG EVANS RAT; MALE; MATERNAL DEPRIVATION; NEWBORN; PREGNANCY; PSYCHOLOGY; RAT; TIME; ULTRASOUND; VOCALIZATION;

ANIMALS; ANIMALS, NEWBORN; FEMALE; MALE; MATERNAL DEPRIVATION; PREGNANCY; RATS; RATS, LONG-EVANS; TIME FACTORS; ULTRASONICS; VOCALIZATION, ANIMAL;

EID: 84919964377     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.21258     Document Type: Article

References (42)

1. Bignall, K. E., Heggeness, F. W., & Palmer, J. E. ( 1974). Effects of acute starvation on cold-induced thermogenesis in the preweanling rat. American Journal of Physiology, 227(5), 1088-1093.
2. Bowers, J. M., Perez-Pouchoulen, M., Edwards, N. S., & McCarthy, M. M. ( 2013). Foxp2 mediates sex differences in ultrasonic vocalization by rat pups and directs order of maternal retrieval. Journal of Neuroscience, 33(8), 3276-3283.
3. Brunelli, S. A., Masmela, J. R., Shair, H. N., & Hofer, M. A. ( 1998) Effects of biparental rearing on ultrasonic vocalization (USV) responses of rat pups (Rattus norvegicus). Journal of Comparative Psychology, 112(4), 331-343.
4. Brunelli, S. A., Shair, H. N., & Hofer, M. A. ( 1994). Hypothermic vocalizations of rat pups (Rattus norvegicus) elicit and direct maternal search behavior. Journal of Comparative Psychology, 108(3), 298-303.
5. Brunelli, S. A., Vinocur, D. D., Soo-Hoo, D., & Hofer, M. A. ( 1997). Five generations of selective breeding for ultrasonic vocalization (USV) responses in N:NIH strain rats. Developmental Psychobiology, 31(4), 255-256.
6. Colonnello, V., Iacobucci, P., & Newberry, R. C. ( 2009). Vocal and locomotor responses of piglets to social isolation and reunion. Developmental Psychobiology, 52(1), 1-12.
7. Fuchs, T., Iacobucci, P., MacKinnon, K. M., & Panksepp, J. ( 2010). Infant-mother recognition in a social rodent (Octodon degus). Journal of Comparative Psychology, 124(2), 166-175.
8. Hennessy, M. B., Miller, E. E., & Shair, H. N. ( 2006). Brief exposure to the biological mother "potentiates" the isolation behavior of precocial Guinea pig pups. Developmental Psychobiology, 48(8), 653-659.
9. Hofer, M. A. ( 1994). Hidden regulators in attachment, separation, and loss. Monographs of the Society for Research in Child Development, 59, 192-207.
10. Hofer, M. A. ( 1996). Multiple regulators of ultrasonic vocalization in the infant rat. Psychoneuroendocrinology, 21(2), 203-217.
11. Hofer, M. A., Brunelli, S. A., Masmela, J. R., & Shair, H. N. ( 1996). Maternal interactions prior to separation potentiate isolation-induced calling in rat pups. Behavioral Neuroscience, 110(5), 1158-1167.
12. Hofer, M. A., Masmela, J. R., Brunelli, S. A., & Shair, H. N. ( 1998). The ontogeny of maternal potentiation of the infant rats' isolation call. Developmental Psychobiology, 33(3), 189-201.
13. Hofer, M. A., & Shair, H. ( 1980). Sensory processes in the control of isolation-induced ultrasonic vocalization by 2-week-old rats. Journal of Comparative and Physiological Psychology, 94(2), 271-279.
14. Hofer, M. A., & Shair, H. N. ( 1978). Ultrasonic vocalization during social interaction and isolation in 2-week-old rats. Developmental Psychobiology, 11(5), 495-504.
15. Hofer, M. A., & Shair, H. N. ( 1992). Ultrasonic vocalization by rat pups during recovery from deep hypothermia. Developmental Psychobiology, 25(7), 511-528.
16. Iijima, M., Yoshimizu, T., Shimazaki, T., Tokugawa, K., Fukumoto, K., & Kurosu, S., et al. Antidepressant and anxiolytic profiles of newly synthesized arginine vasopressin V1B receptor antagonists: TASP0233278 and TASP0390325. British Journal of Pharmacology, 171(14), 3511-3525.
17. Kehoe, P., & 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.
18. Kraebel, K. S., Brasser, S. M., Campbell, J. O., Spear, L. P., & Spear, N. E. ( 2002). Developmental differences in temporal patterns and potentiation of isolation-induced ultrasonic vocalizations: influence of temperature variables. Developmental Psychobiology, 40(2), 147-159.
19. Miczek, K. A., Weerts, E. M., Vivian, J. A., & Barros, H. M. ( 1995). Aggression, anxiety and vocalizations in animals: GABAA and 5-HT anxiolytics. Psychopharmacology, 121(1), 38-56.
20. Moles, A., Kieffer, B. L., & D'Amato, F. R. ( 2004). Deficit in attachment behavior in mice lacking the mu-opioid receptor gene. Science, 304(5679), 1983-1986.
21. Muller, J. M., Moore, H., Myers, M. M., & Shair, H. N. ( 2008). Ventral striatum dopamine D2 receptor activity inhibits rat pups' vocalization response to loss of maternal contact. Behavioral Neuroscience, 122(1), 119-128.
22. Muller, J. M., Moore, H., Myers, M. M., & Shair, H. N. ( 2009). Dopamine's role in social modulation of infant isolation-induced vocalization: II. Maternally modulated infant separation responses are regulated by D1- and D2-family dopamine receptors. Developmental Psychobiology, 51(2), 158-172.
23. Oswalt, G. L., & Meier, G. W. ( 1975). Olfactory, thermal, and tactual influences on infantile ultrasonic vocalization in rats. Developmental Psychobiology, 8(2), 129-135.
24. Ricceri, L., Cutuli, D., Venerosi, A., Scattoni, M. L., & Calamandrei, G. ( 2007). Neonatal basal forebrain cholinergic hypofunction affects ultrasonic vocalizations and fear conditioning responses in preweaning rats. Behavioural Brain Research, 183(1), 111-117.
25. Scattoni, M. L., Crawley, J., & Ricceri, L. ( 2009). Ultrasonic vocalizations: a tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neuroscience and Biobehavioral Reviews, 33(4), 508-515.
26. Shair, H. N. ( 2007). Acquisition and expression of a socially mediated separation response. Behavioural Brain Research, 182(2), 180-192.
27. Shair, H. N. ( 2014). Parental potentiation of vocalization as a marker for filial bonds in infant animals. Developmental Psychobiology.
28. Shair, H. N., Brunelli, S. A., & Hofer, M. A. ( 2005). Lack of evidence for mu-opioid regulation of a socially mediated separation response. Physiology and Behavior, 83(5), 767-767.
29. Shair, H. N., Brunelli, S. A., Masmela, J. R., Boone, E., & Hofer, M. A. ( 2003). Social, thermal, and temporal influences on isolation-induced and maternally potentiated ultrasonic vocalizations of rat pups. Developmental Psychobiology, 42(2), 206-222.
30. Shair, H. N., Masmela, J. R., & Hofer, M. A. ( 1999). The influence of olfaction on potentiation and inhibition of ultrasonic vocalization of rat pups. Physiology and Behavior, 65(4-5), 769-772.
31. Shair, H. N., Muller, J. M., & Moore, H. ( 2009). Dopamine's role in social modulation of infant isolation-induced vocalization: I. Reunion responses to the dam, but not littermates, are dopamine dependent. Developmental Psychobiology, 51(2), 131-146.
32. Shair, H. N., Smith, J. A., & Welch, M. G. ( 2012). Cutting the vagus nerve below the diaphragm prevents maternal potentiation of infant rat vocalization. Developmental Psychobiology, 54(1), 70-76.
33. Smotherman, W. P., Bell, R. W., Starzec, J., Elias, J., & Zachman, T. A. ( 1974). Maternal responses to infant vocalizations and olfactory cues in rats and mice. Behavioral Biology, 12(1), 55-66.
34. Sullivan, R. M., & Toubas, P. ( 1998). Clinical usefulness of maternal odor in newborns: soothing and feeding preparatory responses. Biology of the Neonate, 74(6), 402-408.
35. Varendi, H., Christensson, K., Porter, R. H., & Winberg, J. ( 1998). Soothing effect of amniotic fluid smell in newborn infants. Early Human Development, 51(1), 47-55.
36. Welch, M. G. ( 1988). Holding Time: How to Eliminate Conflict, Temper Tantrums, and Sibling Rivalry and Raise Happy, Loving, Successful Children. New York: Simon and Schuster.
37. Welch, M. G. ( 1992). Holding Time: How to Eliminate Conflict, Temper Tantrums, and Sibling Rivalry and Raise Happy, Loving, Successful Children. New York: Simon and Schuster, Japanese Edition.
38. Welch, M. G., Hofer, M. A., Brunelli, S. A., Stark, R. I., Andrews, H. F., & Austin, J., et al. ( 2012). Family nurture intervention (FNI): methods and treatment protocol of a randomized controlled trial in the NICU. BMC Pediatrics, 12, 14.
39. Welch, M. G., Hofer, M. A., Stark, R. I., Andrews, H. F., Austin, J., & Glickstein, S. B., et al. ( 2013). Randomized controlled trial of Family Nurture Intervention in the NICU: Assessments of length of stay, feasibility and safety. BMC Pediatrics, 13, 148.
40. Welch, M. G., Myers, M. M., Grieve, P. G., Isler, J. R., Fifer, W. P., & Sahni, R., et al. ( 2014). Electroencephalographic activity of preterm infants is increased by Family Nurture Intervention: A randomized controlled trial in the NICU. Clinical Neurophysiology, 125(4), 675-684.
41. Young, D. M., Schenk, A. K., Yang, S. B., Jan, Y. N., & Jan, L. Y. ( 2010). Altered ultrasonic vocalizations in a tuberous sclerosis mouse model of autism. Proceedings of the National Academy of Sciences of the United States of America, 107(24), 11074-11079.
42. Zimmerberg, B., Brunelli, S. A., & Hofer, M. A. ( 1994). Reduction of rat pup ultrasonic vocalizations by the neuroactive steroid allopregnanolone. Pharmacology Biochemistry & Behavior, 47(3), 735-738.