Developmental Neuroscience

Bigelow L.J. · Pope E.K. · Knight J.B. · Rock J.E. · MacLeod S.K. · Bernard P.B.

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Department of Biomedical Sciences, University of Prince Edward Island, Charlottetown, PE, Canada

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Article / Publication Details

First-Page Preview

Received: April 19, 2022
Accepted: June 30, 2022
Published online: July 18, 2022

Number of Print Pages: 9
Number of Figures: 6
Number of Tables: 0

ISSN: 0378-5866 (Print)
eISSN: 1421-9859 (Online)

For additional information: https://www.karger.com/DNE

Abstract

Early-life experiences are critical modifiers of development. An important component of early-life experience is the nature of maternal interactions, which can be modified by stress. During rearing, mothers are typically allocated to single-level cages where they are readily accessible to pups, a potentially stressful scenario not reflective of nature. Accordingly, mothers regularly removed from the rearing environment interact differently with their offspring, leading to long-term changes in offspring physiology and behavior. Such changes commonly include modifications within the hypothalamic-pituitary-adrenal axis, of which corticosterone is a major component. Modifications in the hypothalamic-pituitary-adrenal axis may also be manifested through changes in affective behavior and assessed via tests such as the open field and elevated plus maze as well as via ultrasonic vocalization (USV) analysis. As a means of assessing the impact of rearing in a shelved environment, we allocated mothers to standard single-level cages or cages with an integrated shelf, which allowed the mother to temporarily escape pups. While there were no differences in fecal cortico­sterone, behavior in the elevated plus maze, or USVs, male rats reared in standard cages weighed more, and all standard single-level housed rats spent more time in the center of the open field. The observed differences indicate that allocating nursing mothers to shelved environments throughout the postnatal period has long-lasting effects on offspring behavior that must be considered when establishing dam enrichment protocols.

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References Korosi A, Baram TZ. The pathways from mother’s love to baby’s future. Front Behav Neurosci. 2009;3:27. Orso R, Creutzberg KC, Wearick-Silva LE, Wendt Viola T, Tractenberg SG, Benetti F, et al. How early life stress impact maternal care: a systematic review of rodent studies. Front Behav Neurosci. 2019 Aug 28;13:197. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res. 2000 Jan;122:81–103. Gaskill BN, Pritchett-Corning KR. Effect of cage space on behavior and reproduction in crl:CD(SD) and BN/crl laboratory rats. J Am Assoc Lab Anim Sci. 2015 Sep;54(5):497–506. Chen Y, Baram TZ. Toward understanding how early-life stress reprograms cognitive and emotional brain networks. Neuropsychopharmacol. 2016 Jan;41(1):197–206. Ratuski AS, Weary DM. A break from the pups: the effects of loft access on the welfare of lactating laboratory rats. PLoS One. 2021 Jun 8;16(6):e0253020. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Rev. 2000 Feb 1;21(1):55–89. Aisa B, Tordera R, Lasheras B, Del Río J, Ramírez MJ. Effects of maternal separation on hypothalamic-pituitary-adrenal responses, cognition and vulnerability to stress in adult female rats. Neuroscience. 2008 Jul;154(4):1218–26. Lundberg S, Martinsson M, Nylander I, Roman E. Altered corticosterone levels and social play behavior after prolonged maternal separation in adolescent male but not female Wistar rats. Horm Behav. 2017 Jan;87:137–44. Pinheiro ML, Ferraz-de-Paula V, Ribeiro A, Sakai M, Bernardi MM, Palermo-Neto J. Long-term maternal separation differentially alters serum corticosterone levels and blood neutrophil activity in A/J and C57BL/6 mouse offspring. Neuroimmunomodulation. 2011;18(3):184–90. Roque S, Mesquita AR, Palha JA, Sousa N, Correia-Neves M. The behavioral and immunological impact of maternal separation: a matter of timing. Front Behav Neurosci. 2014 May 22;8:192. Mendl M, Burman OHP, Paul ES. An integrative and functional framework for the study of animal emotion and mood. Proc R Soc B. 2010 Oct 7;277(1696):2895–904. Rowland NE, Toth LA. Analytic and interpretational pitfalls to measuring fecal corticosterone metabolites in laboratory rats and mice. Comp Med. 2019 Oct 1;69(5):337–49. Huot RL, Thrivikraman KV, Meaney MJ, Plotsky PM. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology. 2001 Dec 1;158(4):366–73. Kalinichev M, Easterling KW, Plotsky PM, Holtzman SG. Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol Biochem Behav. 2002 Aug;73(1):131–40. McIntosh J, Anisman H, Merali Z. Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Brain Res Dev Brain Res. 1999 Mar;113(1–2):97–106. Wigger A, Neumann ID. Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol Behav. 1999 Apr;66(2):293–302. Walsh RN, Cummins RA. The open-field test: a critical review. Psychol Bull. 1976 May;83(3):482–504. Portfors CV. Types and functions of ultrasonic vocalizations in laboratory rats and mice. J Am Assoc Lab Anim Sci. 2007 Jan;46(1):28–34. Wright JM, Gourdon JC, Clarke PBS. Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: effects of amphetamine and social context. Psychopharmacology. 2010 Jul;211(1):1–13. Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc. 2007 Feb;2(2):322–8. Hall CS. Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J Comp Psychol. 1934;18(3):385–403. Vahl TP, Ulrich-Lai YM, Ostrander MM, Dolgas CM, Elfers EE, Seeley RJ, et al. Comparative analysis of ACTH and corticosterone sampling methods in rats. Am J Physiol Endocrinol Metab. 2005 Nov;289(5):E823–8. Meaney MJ, Aitken DH, Sharma S, Viau V. Basal ACTH, corticosterone and corticosterone-binding globulin levels over the diurnal cycle, and age-related changes in hippocampal type I and type II corticosteroid receptor binding capacity in young and aged, handled and nonhandled rats. Neuroendocrinology. 1992;55(2):204–13. Meyer N, Kröger M, Thümmler J, Tietze L, Palme R, Touma C. Impact of three commonly used blood sampling techniques on the welfare of laboratory mice: taking the animal’s perspective. PLoS One. 2020 Sep 8;15(9):e0238895. Tuli JS, Smith JA, Morton DB. Corticosterone, adrenal and spleen weight in mice after tail bleeding, and its effect on nearby animals. Lab Anim. 1995 Jan 1;29(1):90–5. Abelson KSP, Adem B, Royo F, Carlsson H-E, Hau J. High plasma corticosterone levels persist during frequent automatic blood sampling in rats. In Vivo. 2005 Sep–Oct;19(5):815–9. Bamberg E, Palme R, Meingassner JG. Excretion of corticosteroid metabolites in urine and faeces of rats. Lab Anim. 2001 Oct 1;35(4):307–14. Lepschy M, Touma C, Hruby R, Palme R. Non-invasive measurement of adrenocortical activity in male and female rats. Lab Anim. 2007 Jul 1;41(3):372–87. Lehmann J, Feldon J. Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing? Rev Neurosci. 2000 Jan;11(4):383–408. Komada M, Takao K, Miyakawa T. Elevated plus maze for mice. J Vis Exp. 2008 Dec 22;(22):1088. Mak P, Broussard C, Vacy K, Broadbear JH. Modulation of anxiety behavior in the elevated plus maze using peptidic oxytocin and vasopressin receptor ligands in the rat. J Psychopharmacol. 2012 Apr;26(4):532–42. Sobin C, Golub M. Behavioral outcome as a primary organizing principle for mechanistic data in developmental neurotoxicity. In: Slikker W Jr, Wang C, Paule MG, eds. Handbook of Developmental Neurotoxicology. New York, NY: Elsevier; 2018, p. 337–47. Nakade Y, Mantyh C, Pappas TN, Takahashi T. Fecal pellet output does not always correlate with colonic transit in response to restraint stress and corticotropin-releasing factor in rats. J Gastroenterol. 2007 Apr 26;42(4):279–82. Hunt HF, Otis LS. Conditioned and unconditioned emotional defectation in the rat. J Comp Physiol Psychol. 1953;46(5):378–82. Archer J. Tests for emotionality in rats and mice: a review. Anim Behav. 1973 May;21(2):205–35. Pare WP. Relationship of various behaviors in the open-field test of emotionality. Psychol Rep. 1964 Feb;14(1):19–22. Ramos A, Pereira E, Martins GC, Wehrmeister TD, Izídio GS. Integrating the open field, elevated plus maze and light/dark box to assess different types of emotional behaviors in one single trial. Behav Brain Res. 2008 Nov;193(2):277–88. Carobrez AP, Bertoglio LJ. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev. 2005 Jan;29(8):1193–205. Mason GJ. Stereotypies: a critical review. Anim Behav. 1991 Jun;41(6):1015–37. Lippmann M, Bress A, Nemeroff CB, Plotsky PM, Monteggia LM. Long-term behavioural and molecular alterations associated with maternal separation in rats: molecular adaptations after maternal separation. Eur J Neurosci. 2007 Jun 6;25(10):3091–8. Bigelow LJ, Cohen AJ, Pimm R, Knight JB, Bernard PB. Ultrasonic vocalization analysis as a novel metric to assess cage enrichment in rats. J Am Assoc Lab Anim Sci. 2022;61(2):140–8. Article / Publication Details

First-Page Preview

Received: April 19, 2022
Accepted: June 30, 2022
Published online: July 18, 2022

Number of Print Pages: 9
Number of Figures: 6
Number of Tables: 0

ISSN: 0378-5866 (Print)
eISSN: 1421-9859 (Online)

For additional information: https://www.karger.com/DNE

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