Maternal separation with neonatal pain influences later-life fear conditioning and somatosenation in male and female rats

References

• Alves, R. L., Portugal, C. C., Summavielle, T., Barbosa, F., & Magalhães, A. (2019). Maternal separation effects on mother rodents’ behaviour: A systematic review. Neuroscience and Biobehavioral Reviews. Advance online publication. https://doi.org/10.1016/j.neubiorev.2019.09.008
   Google Scholar
• Anand, K. J., & Scalzo, F. M. (2000). Can adverse neonatal experiences alter brain development and subsequent behavior? Biology of the Neonate, 77(2), 69–82. https://doi.org/10.1159/000014197
   PubMedGoogle Scholar
• Anand, K. J. S., Coskun, V., Thrivikraman, K. V., Nemeroff, C. B., & Plotsky, P. M. (1999). Long-term behavioral effects of repetitive pain in neonatal rat pups. Physiology & Behavior, 66(4), 627–637. https://doi.org/10.1016/S0031-9384(98)00338-2
   PubMed Web of Science ®Google Scholar
• Barker, D. P., & Rutter, N. (1995). Exposure to invasive procedures in neonatal intensive care unit admissions. Archives of Disease in Childhood. Fetal and Neonatal Edition, 72(1), F47–F48. https://doi.org/10.1136/fn.72.1.f47
   PubMed Web of Science ®Google Scholar
• Beane, M. L., Cole, M. A., Spencer, R. L., & Rudy, J. W. (2002). Neonatal handling enhances contextual fear conditioning and alters corticosterone stress responses in young rats. Hormones and Behavior, 41(1), 33–40. https://doi.org/10.1006/hbeh.2001.1725
   PubMed Web of Science ®Google Scholar
• Bhutta, A. T., Rovnaghi, C., Simpson, P. M., Gossett, J. M., Scalzo, F. M., & Anand, K. J. (2001). Interactions of inflammatory pain and morphine in infant rats: Long-term behavioral effects. Physiology & Behavior, 73(1–2), 51–58. https://doi.org/10.1016/s0031-9384(01)00432-2
   PubMed Web of Science ®Google Scholar
• Bonin, R. P., Bories, C., & De Koninck, Y. (2014). A simplified up-down method (SUDO) for measuring mechanical nociception in rodents using von Frey filaments. Molecular Pain, 10, 26. https://doi.org/10.1186/1744-8069-10-26
   PubMed Web of Science ®Google Scholar
• Brummelte, S., Grunau, R. E., Chau, V., Poskitt, K. J., Brant, R., Vinall, J., Gover, A., Synnes, A. R., & Miller, S. P. (2012). Procedural pain and brain development in premature newborns. Annals of Neurology, 71(3), 385–396. https://doi.org/10.1002/ana.22267
   PubMed Web of Science ®Google Scholar
• Burman, M. A., & Gewirtz, J. C. (2007). Hippocampal activity, but not plasticity, is required for early consolidation of fear conditioning with a short trace interval. The European Journal of Neuroscience, 25(8), 2483–2490. https://doi.org/10.1111/j.1460-9568.2007.05493.x
   PubMed Web of Science ®Google Scholar
• Carbajal, R., Rousset, A., Danan, C., Coquery, S., Nolent, P., Ducrocq, S., Saizou, C., Lapillonne, A., Granier, M., Durand, P., Lenclen, R., Coursol, A., Hubert, P., de Saint Blanquat, L., Boëlle, P.-Y., Annequin, D., Cimerman, P., Anand, K. J. S., & Bréart, G. (2008). Epidemiology and treatment of painful procedures in neonates in intensive care units. JAMA, 300(1), 60–70. https://doi.org/10.1001/jama.300.1.60
   PubMed Web of Science ®Google Scholar
• Carmo, E. d C. D., Sanada, L. S., Machado, N. L. B., & Fazan, V. P. S. (2016). Does pain in the neonatal period influence motor and sensory functions in a similar way for males and females during post-natal development in rats? Pain Medicine, 17(8), 1520–1529. https://doi.org/10.1093/pm/pnv117
   PubMed Web of Science ®Google Scholar
• Chaplan, S. R., Bach, F. W., Pogrel, J. W., Chung, J. M., & Yaksh, T. L. (1994). Quantitative assessment of tactile allodynia in the rat paw. Journal of Neuroscience Methods, 53(1), 55–63. https://doi.org/10.1016/0165-0270(94)90144-9
   PubMed Web of Science ®Google Scholar
• Chen, M., Xia, D., Min, C., Zhao, X., Chen, Y., Liu, L., & Li, X. (2016). Neonatal repetitive pain in rats leads to impaired spatial learning and dysregulated hypothalamic-pituitary-adrenal axis function in later life. Scientific Reports, 6(1), 39159. https://doi.org/10.1038/srep39159
   PubMedGoogle Scholar
• Chocyk, A., Przyborowska, A., Makuch, W., Majcher-Maślanka, I., Dudys, D., & Wędzony, K. (2014). The effects of early-life adversity on fear memories in adolescent rats and their persistence into adulthood. Behavioural Brain Research, 264, 161–172. https://doi.org/10.1016/j.bbr.2014.01.040 24508235
   PubMed Web of Science ®Google Scholar
• Cruz, M. D., Fernandes, A. M., & Oliveira, C. R. (2016). Epidemiology of painful procedures performed in neonates: A systematic review of observational studies. European Journal of Pain, 20(4), 489–498. https://doi.org/10.1002/ejp.757
   PubMed Web of Science ®Google Scholar
• Daniels, W. M. U., Pietersen, C. Y., Carstens, M. E., & Stein, D. J. (2004). Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metabolic Brain Disease, 19(1–2), 3–14. https://doi.org/10.1023/B:MEBR.0000027412.19664.b3
   PubMed Web of Science ®Google Scholar
• Davis, S. M., Rice, M., & Burman, M. A. (2020). Inflammatory neonatal pain disrupts maternal behavior and subsequent fear conditioning in a rodent model. Developmental Psychobiology, 62(1), 88–98. https://doi.org/10.1002/dev.21889
   PubMed Web of Science ®Google Scholar
• Davis, S. M., Rice, M., Rudlong, J., Eaton, V., King, T., & Burman, M. A. (2018). Neonatal pain and stress disrupts later-life pavlovian fear conditioning and sensory function in rats: Evidence for a two-hit model. Developmental Psychobiology, 60(5), 520–533. https://doi.org/10.1002/dev.21632
   PubMed Web of Science ®Google Scholar
• Deal, A. L., Erickson, K. J., Shiers, S. I., & Burman, M. A. (2016). Limbic system development underlies the emergence of classical fear conditioning during the third and fourth weeks of life in the rat. Behavioral Neuroscience, 130(2), 212–230. https://doi.org/10.1037/bne0000130
   PubMed Web of Science ®Google Scholar
• Diorio, D., Viau, V., & Meaney, M. J. (1993). The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. The Journal of Neuroscience, 13(9), 3839–3847. https://doi.org/10.1523/JNEUROSCI.13-09-03839.1993
   PubMed Web of Science ®Google Scholar
• Fitzgerald, M. (2005). The development of nociceptive circuits. Nature Reviews. Neuroscience, 6(7), 507–520. https://doi.org/10.1038/nrn1701
   PubMed Web of Science ®Google Scholar
• Fuentes, I. M., Walker, N. K., Pierce, A. N., Holt, B. R., Di Silvestro, E. R., & Christianson, J. A. (2016). Neonatal maternal separation increases susceptibility to experimental colitis and acute stress exposure in male mice. IBRO Reports, 1, 10–18. https://doi.org/10.1016/j.ibror.2016.07.001
   PubMedGoogle Scholar
• Grunau, R. E., Holsti, L., & Peters, J. W. B. (2006). Long-term consequences of pain in human neonates. Seminars in Fetal & Neonatal Medicine, 11(4), 268–275. https://doi.org/10.1016/j.siny.2006.02.007
   PubMed Web of Science ®Google Scholar
• Hall, R. W., & Anand, K. J. S. (2005). Short- and long-term impact of neonatal pain and stress: More than an ouchie. NeoReviews, 6(2), e69–e75. https://doi.org/10.1542/neo.6-2-e69
   Google Scholar
• Hargreaves, K., Dubner, R., Brown, F., Flores, C., & Joris, J. (1988). A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain, 32(1), 77–88. https://doi.org/10.1016/0304-3959(88)90026-7
   PubMed Web of Science ®Google Scholar
• Kalinichev, M., Easterling, K. W., Plotsky, P. M., & Holtzman, S. G. (2002). Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long–Evans rats. Pharmacology, Biochemistry, and Behavior, 73(1), 131–140. https://doi.org/10.1016/S0091-3057(02)00781-5
   PubMed Web of Science ®Google Scholar
• LaPrairie, J. L., & Murphy, A. Z. (2007). Female rats are more vulnerable to the long-term consequences of neonatal inflammatory injury. Pain, 132, S124–S133. https://doi.org/10.1016/j.pain.2007.08.010
   Web of Science ®Google Scholar
• Lehmann, J., & Feldon, J. (2000). Long-term biobehavioral effects of maternal separation in the rat: Consistent or confusing? Reviews in the Neurosciences, 11(4), 383–408. https://doi.org/10.1515/revneuro.2000.11.4.383
   PubMed Web of Science ®Google Scholar
• Lehmann, J., Pryce, C. R., Bettschen, D., & Feldon, J. (1999). The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacology, Biochemistry, and Behavior, 64(4), 705–715. https://doi.org/10.1016/S0091-3057(99)00150-1
   PubMed Web of Science ®Google Scholar
• Lidow, M. S. (2002). Long-term effects of neonatal pain on nociceptive systems. Pain, 99(3), 377–383. https://doi.org/10.1016/s0304-3959(02)00258-0
   PubMed Web of Science ®Google Scholar
• Mizoguchi, H., Fukumoto, K., Sakamoto, G., Jin, S., Toyama, A., Wang, T., Suzumura, A., & Sato, J. (2019). Maternal separation as a risk factor for aggravation of neuropathic pain in later life in mice. Behavioural Brain Research, 359, 942–949. https://doi.org/10.1016/j.bbr.2018.06.015
   PubMed Web of Science ®Google Scholar
• Mooney-Leber, S. M., & Brummelte, S. (2017). Neonatal pain and reduced maternal care: Early-life stressors interacting to impact brain and behavioral development. Neuroscience, 342, 21–36. https://doi.org/10.1016/j.neuroscience.2016.05.001
   PubMed Web of Science ®Google Scholar
• Mooney-Leber, S. M., & Brummelte, S. (2020). Neonatal pain and reduced maternal care alter adult behavior and hypothalamic-pituitary-adrenal axis reactivity in a sex-specific manner. Developmental Psychobiology, 62(5), 631–643. https://doi.org/10.1002/dev.21941
   PubMed Web of Science ®Google Scholar
• Mooney-Leber, S. M., Spielmann, S. S., & Brummelte, S. (2018). Repetitive neonatal pain and reduced maternal care alter brain neurochemistry. Developmental Psychobiology, 60(8), 963–974. https://doi.org/10.1002/dev.21777
   PubMed Web of Science ®Google Scholar
• Page, G. G., Blakely, W. P., & Kim, M. (2005). The impact of early repeated pain experiences on stress responsiveness and emotionality at maturity in rats. Brain, Behavior, and Immunity, 19(1), 78–87. https://doi.org/10.1016/j.bbi.2004.05.002
   PubMed Web of Science ®Google Scholar
• Pao, M., & Bosk, A. (2011). Anxiety in medically ill children/adolescents. Depression and Anxiety, 28(1), 40–49. https://doi.org/10.1002/da.20727
   PubMed Web of Science ®Google Scholar
• Phillips, R. G., & LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience, 106(2), 274–285. https://doi.org/10.1037//0735-7044.106.2.274
   PubMed Web of Science ®Google Scholar
• Roofthooft, D. W. E., Simons, S. H. P., Anand, K. J. S., Tibboel, D., & van Dijk, M. (2014). Eight years later, are we still hurting newborn infants? Neonatology, 105(3), 218–226. https://doi.org/10.1159/000357207
   PubMed Web of Science ®Google Scholar
• Salberg, S., Noel, M., Burke, N. N., Vinall, J., & Mychasiuk, R. (2020). Utilization of a rodent model to examine the neurological effects of early life adversity on adolescent pain sensitivity. Developmental Psychobiology, 62(3), 386–399. https://doi.org/10.1002/dev.21922
   PubMed Web of Science ®Google Scholar
• Sampath, D., Sabitha, K. R., Hegde, P., Jayakrishnan, H. R., Kutty, B. M., Chattarji, S., Rangarajan, G., & Laxmi, T. R. (2014). A study on fear memory retrieval and REM sleep in maternal separation and isolation stressed rats. Behavioural Brain Research, 273, 144–154. https://doi.org/10.1016/j.bbr.2014.07.034
   PubMed Web of Science ®Google Scholar
• Schwaller, F., & Fitzgerald, M. (2014). The consequences of pain in early life: Injury‐induced plasticity in developing pain pathways. The European Journal of Neuroscience, 39(3), 344–352. http://doi.org/10.1111/[email protected]/(ISSN)1460-9568.brain_awareness_week https://doi.org/10.1111/ejn.12414
   PubMed Web of Science ®Google Scholar
• Sevelinges, Y., Sullivan, R. M., Messaoudi, B., & Mouly, A.-M. (2008). Neonatal odor-shock conditioning alters the neural network involved in odor fear learning at adulthood. Learning & Memory, 15(9), 649–656. https://doi.org/10.1101/lm.998508
   PubMed Web of Science ®Google Scholar
• Shimada, C., Kurumiya, S., Noguchi, Y., & Umemoto, M. (1990). The effect of neonatal exposure to chronic footshock on pain-responsiveness and sensitivity to morphine after maturation in the rat. Behavioural Brain Research, 36(1–2), 105–111. https://doi.org/10.1016/0166-4328(90)90165-B
   PubMed Web of Science ®Google Scholar
• Stevenson, C. W., Spicer, C. H., Mason, R., & Marsden, C. A. (2009). Early life programming of fear conditioning and extinction in adult male rats. Behavioural Brain Research, 205(2), 505–510. https://doi.org/10.1016/j.bbr.2009.08.005 19682501
   PubMed Web of Science ®Google Scholar
• Taddio, A., Katz, J., Ilersich, A. L., & Koren, G. (1997). Effect of neonatal circumcision on pain response during subsequent routine vaccination. The Lancet, 349(9052), 599–603. https://doi.org/10.1016/S0140-6736(96)10316-0
   PubMed Web of Science ®Google Scholar
• Toda, H., Boku, S., Nakagawa, S., Inoue, T., Kato, A., Takamura, N., Song, N., Nibuya, M., Koyama, T., & Kusumi, I. (2014). Maternal separation enhances conditioned fear and decreases the mRNA levels of the neurotensin receptor 1 gene with hypermethylation of this gene in the rat amygdala. PLoS One, 9(5), e97421. https://doi.org/10.1371/journal.pone.0097421
   PubMed Web of Science ®Google Scholar
• van den Hoogen, N. J., Patijn, J., Tibboel, D., Joosten, B. A., Fitzgerald, M., & Kwok, C. H. T. (2018). Repeated touch and needle-prick stimulation in the neonatal period increases the baseline mechanical sensitivity and postinjury hypersensitivity of adult spinal sensory neurons. Pain, 159(6), 1166–1175. https://doi.org/10.1097/j.pain.0000000000001201
   PubMed Web of Science ®Google Scholar
• van den Hoogen, N. J., Patijn, J., Tibboel, D., & Joosten, E. A. (2020). Repetitive noxious stimuli during early development affect acute and long-term mechanical sensitivity in rats. Pediatric Research, 87(1), 26–31. https://doi.org/10.1038/s41390-019-0420-x
   PubMed Web of Science ®Google Scholar
• Victoria, N. C., & Murphy, A. Z. (2016). The long-term impact of early life pain on adult responses to anxiety and stress: Historical perspectives and empirical evidence. Experimental Neurology, 275, 261–273. https://doi.org/10.1016/j.expneurol.2015.07.017
   PubMed Web of Science ®Google Scholar
• Vilela, F. C., Vieira, J. S., Giusti-Paiva, A., & Silva, M. L. D. (2017). Experiencing early life maternal separation increases pain sensitivity in adult offspring. International Journal of Developmental Neuroscience, 62(1), 8–14. https://doi.org/10.1016/j.ijdevneu.2017.07.003
   PubMedGoogle Scholar
• Walker, S. M. (2019). Long-term effects of neonatal pain. Seminars in Fetal & Neonatal Medicine, 24(4), 101005. https://doi.org/10.1016/j.siny.2019.04.005
   PubMed Web of Science ®Google Scholar
• Walker, S. M., Melbourne, A., O’Reilly, H., Beckmann, J., Eaton-Rosen, Z., Ourselin, S., & Marlow, N. (2018). Somatosensory function and pain in extremely preterm young adults from the UK EPICure cohort: Sex-dependent differences and impact of neonatal surgery. British Journal of Anaesthesia, 121(3), 623–635. https://doi.org/10.1016/j.bja.2018.03.035
   PubMed Web of Science ®Google Scholar
• Weaver, S. A., Diorio, J., & Meaney, M. J. (2007). Maternal separation leads to persistent reductions in pain sensitivity in female rats. The Journal of Pain, 8(12), 962–969. https://doi.org/10.1016/j.jpain.2007.07.001
   PubMed Web of Science ®Google Scholar
• Williams, M. D., & Lascelles, B. D. X. (2020). Early neonatal pain-A review of clinical and experimental implications on painful conditions later in life. Frontiers in Pediatrics, 8, 30. https://doi.org/10.3389/fped.2020.00030
   PubMed Web of Science ®Google Scholar
• Zuke, J. T., Rice, M., Rudlong, J., Paquin, T., Russo, E., & Burman, M. A. (2019). The effects of acute neonatal pain on expression of corticotropin releasing hormone and juvenile anxiety in a rodent model. eNeuro, 6(6), 0162–19. https://doi.org/10.1523/ENEURO.0162-19.2019
   Google Scholar