Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-27T03:08:56.278Z Has data issue: false hasContentIssue false
  • English
  • Français

Growth restriction alters adult spatial memory and sensorimotor gating in a sex-specific manner

Published online by Cambridge University Press:  05 December 2011

B. Lauritz ,
A. L. Siebel ,
V. Guille ,
A. J. Jefferies  and
M. E. Wlodek
B. Lauritz
Affiliation:
Department of Physiology, The University of Melbourne, Parkville, Vic., Australia
A. L. Siebel
Affiliation:
Department of Physiology, The University of Melbourne, Parkville, Vic., Australia
V. Guille
Affiliation:
Integrative Neuroscience Facility, Howard Florey Institute, The University of Melbourne, Parkville, Vic., Australia
A. J. Jefferies
Affiliation:
Department of Physiology, The University of Melbourne, Parkville, Vic., Australia
M. E. Wlodek*
Affiliation:
Department of Physiology, The University of Melbourne, Parkville, Vic., Australia
*
*Address for correspondence: Dr M. E. Wlodek, Department of Physiology, The University of Melbourne, Grattan Street, Parkville, Vic. 3010, Australia. (Email [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

In Western society, impaired uteroplacental blood flow is the major cause of human intrauterine growth restriction. Infants born small and who experience late childhood accelerated growth have an increased risk of developing adult diseases. Recent studies also suggest a link between birth weight and altered adult behavior, particularly relating to motor function, learning and memory, depression and schizophrenia. The aim of this study was to determine the relative influence of prenatal and postnatal growth restriction on adult behavioral outcomes in male and female rats. Uteroplacental insufficiency was induced in Wistar Kyoto rats by bilateral uterine vessel ligation on day 18 of gestation producing growth-restricted offspring (Restricted group). The Control group had sham surgery. Another group underwent sham surgery, with a reduction in litter size to five at birth equivalent to the Restricted litter size (Reduced Litter group). At 6 months of age, a series of behavioral tests were conducted in male and female offspring. Growth restriction did not impair motor function. In fact, Restricted and Reduced Litter males showed enhanced motor performance compared with Controls (P < 0.05). Spatial memory was greater in Restricted females only (P < 0.05). The Porsolts test was unremarkable, however, males exhibited more depressive-like behavior than females (P < 0.05). A reduction in sensorimotor gating function was identified in Reduced Litter males and females (P < 0.05). We have demonstrated that growth restriction and/or a poor lactational environment can affect adult rat behavior, particularly balance and coordination, memory and learning, and sensorimotor gating function, in a sex-specific manner.

Keywords

anxietylearning and memorylow birth weightmotor functionuteroplacental insufficiency
Type
Original Articles
Information
Journal of Developmental Origins of Health and Disease , Volume 3 , Issue 1 , February 2012 , pp. 59 - 68
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

Co-first authors: Contributed equally to this work.

References

1. Barker, DJ. Fetal origins of coronary heart disease. BMJ. 1995; 311, 171–174.CrossRefGoogle ScholarPubMed
2. Martyn, CN, Barker, DJ, Jespersen, S, et al. Growth in utero, adult blood pressure, and arterial compliance. Br Heart J. 1995; 73, 116–121.CrossRefGoogle ScholarPubMed
3. Evensen, KA, Vik, T, Helbostad, J, et al. Motor skills in adolescents with low birth weight. Arch Dis Child Fetal Neonatal Ed. 2004; 89, F451–F455.CrossRefGoogle ScholarPubMed
4. Fattal-Valevski, A, Leitner, Y, Kutai, M, et al. Neurodevelopmental outcome in children with intrauterine growth retardation: a 3-year follow-up. J Child Neurol. 1999; 14, 724–727.CrossRefGoogle ScholarPubMed
5. O'Keeffe, MJ, O'Callaghan, M, Williams, GM, Najman, JM, Bor, W. Learning, cognitive, and attentional problems in adolescents born small for gestational age. Pediatrics. 2003; 112, 301–307.CrossRefGoogle ScholarPubMed
6. Gale, CR, Martyn, CN. Birth weight and later risk of depression in a national birth cohort. Br J Psychiatry. 2004; 184, 28–33.CrossRefGoogle Scholar
7. Susser, ES, Lin, SP. Schizophrenia after prenatal exposure to the Dutch Hunger Winter of 1944–1945. Arch Gen Psychiatry. 1992; 49, 983–988.CrossRefGoogle Scholar
8. Frasure-Smith, N, Lesperance, F. Depression and anxiety as predictors of 2-year cardiac events in patients with stable coronary artery disease. Arch Gen Psychiatry. 2008; 65, 62–71.CrossRefGoogle ScholarPubMed
9. O'Dowd, R, Kent, JC, Moseley, JM, Wlodek, ME. Effects of uteroplacental insufficiency and reducing litter size on maternal mammary function and postnatal offspring growth. Am J Physiol Regul Integr Comp Physiol. 2008; 294, R539–R548.CrossRefGoogle ScholarPubMed
10. Wlodek, ME, Mibus, A, Tan, A, et al. Normal lactational environment restores nephron endowment and prevents hypertension after placental restriction in the rat. J Am Soc Nephrol. 2007; 18, 1688–1696.CrossRefGoogle ScholarPubMed
11. Wlodek, ME, Westcott, KT, O'Dowd, R, et al. Uteroplacental restriction in the rat impairs fetal growth in association with alterations in placental growth factors including PTHrP. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R1620–R1627.CrossRefGoogle ScholarPubMed
12. Wlodek, ME, Westcott, K, Siebel, AL, Owens, JA, Moritz, KM. Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int. 2008; 74, 187–195.CrossRefGoogle ScholarPubMed
13. Siebel, AL, Gallo, LA, Guan, TC, Owens, JA, Wlodek, ME. Cross-fostering and improved lactation ameliorates deficits in endocrine pancreatic morphology in growth-restricted adult male rat offspring. J Dev Orig Health Dis. 2010; 1, 234–244.CrossRefGoogle ScholarPubMed
14. Siebel, AL, Mibus, A, De Blasio, MJ, et al. Improved lactational nutrition and postnatal growth ameliorates impairment of glucose tolerance by uteroplacental insufficiency in male rat offspring. Endocrinology. 2008; 149, 3067–3076.CrossRefGoogle ScholarPubMed
15. Wadley, GD, Siebel, AL, Cooney, GJ, et al. Uteroplacental insufficiency and reducing litter size alters skeletal muscle mitochondrial biogenesis in a sex-specific manner in the adult rat. Am J Physiol Endocrinol Metab. 2008; 294, E861–E869.CrossRefGoogle Scholar
16. Mallard, C, Loeliger, M, Copolov, D, Rees, S. Reduced number of neurons in the hippocampus and the cerebellum in the postnatal guinea-pig following intrauterine growth-restriction. Neuroscience. 2000; 100, 327–333.CrossRefGoogle ScholarPubMed
17. Rees, S, Bocking, AD, Harding, R. Structure of the fetal sheep brain in experimental growth retardation. J Dev Physiol. 1988; 10, 211–225.Google ScholarPubMed
18. Smart, JL, Dobbing, J, Adlard, BP, Lynch, A, Sands, J. Vulnerability of developing brain: relative effects of growth restriction during the fetal and suckling periods on behavior and brain composition of adult rats. J Nutr. 1973; 103, 1327–1338.CrossRefGoogle ScholarPubMed
19. Sommerfelt, K, Andersson, HW, Sonnander, K, et al. Cognitive development of term small for gestational age children at five years of age. Arch Dis Child. 2000; 83, 25–30.CrossRefGoogle ScholarPubMed
20. Morris, RG, Garrud, P, Rawlins, JN, O'Keefe, J. Place navigation impaired in rats with hippocampal lesions. Nature. 1982; 297, 681–683.CrossRefGoogle ScholarPubMed
21. Dellu, F, Mayo, W, Cherkaoui, J, Le Moal, M, Simon, H. A two-trial memory task with automated recording: study in young and aged rats. Brain Res. 1992; 588, 132–139.CrossRefGoogle Scholar
22. Costello, EJ, Worthman, C, Erkanli, A, Angold, A. Prediction from low birth weight to female adolescent depression: a test of competing hypotheses. Arch Gen Psychiatry. 2007; 64, 338–344.CrossRefGoogle ScholarPubMed
23. Pellow, S, Chopin, P, File, SE, Briley, M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods. 1985; 14, 149–167.CrossRefGoogle Scholar
24. Porsolt, RD, Le Pichon, M, Jalfre, M. Depression: a new animal model sensitive to antidepressant treatments. Nature. 1977; 266, 730–732.CrossRefGoogle ScholarPubMed
25. Adori, C, Zelena, D, Timar, J, et al. Intermittent prenatal MDMA exposure alters physiological but not mood related parameters in adult rat offspring. Behav Brain Res. 2009; 206, 299–309.CrossRefGoogle Scholar
26. Wahlbeck, K, Forsen, T, Osmond, C, Barker, DJ, Eriksson, JG. Association of schizophrenia with low maternal body mass index, small size at birth, and thinness during childhood. Arch Gen Psychiatry. 2001; 58, 48–52.CrossRefGoogle ScholarPubMed
27. Grillon, C, Ameli, R, Charney, DS, Krystal, J, Braff, D. Startle gating deficits occur across prepulse intensities in schizophrenic patients. Biol Psychiatry. 1992; 32, 939–943.CrossRefGoogle ScholarPubMed
28. Craft, RM, Clark, JL, Hart, SP, Pinckney, MK. Sex differences in locomotor effects of morphine in the rat. Pharmacol Biochem Behav. 2006; 85, 850–858.CrossRefGoogle ScholarPubMed
29. Rogers, DC, Campbell, CA, Stretton, JL, Mackay, KB. Correlation between motor impairment and infarct volume after permanent and transient middle cerebral artery occlusion in the rat. Stroke. 1997; 28, 2060–2065; discussion 2066.CrossRefGoogle ScholarPubMed
30. Carter, RJ, Lione, LA, Humby, T, et al. Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J Neurosci. 1999; 19, 3248–3257.CrossRefGoogle ScholarPubMed
31. van den Buuse, M, Martin, S, Brosda, J, et al. Enhanced effect of dopaminergic stimulation on prepulse inhibition in mice deficient in the alpha subunit of G(z). Psychopharmacology (Berl). 2005; 183, 358–367.CrossRefGoogle ScholarPubMed
32. Westcott, KT, Hirst, JJ, Ciurej, I, Walker, DW, Wlodek, ME. Brain allopregnanolone in the fetal and postnatal rat in response to uteroplacental insufficiency. Neuroendocrinology. 2008; 88, 287–292.CrossRefGoogle ScholarPubMed
33. Dobbing, J, Sands, J. Quantitative growth and development of human brain. Arch Dis Child. 1973; 48, 757–767.CrossRefGoogle ScholarPubMed
34. Chapillon, P, Lalonde, R, Jones, N, Caston, J. Early development of synchronized walking on the rotorod in rats. Effects of training and handling. Behav Brain Res. 1998; 93, 77–81.CrossRefGoogle ScholarPubMed
35. Frye, CA. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol Behav. 1995; 57, 5–14.CrossRefGoogle Scholar
36. Warren, SG, Juraska, JM. Spatial and nonspatial learning across the rat estrous cycle. Behav Neurosci. 1997; 111, 259–266.CrossRefGoogle ScholarPubMed
37. Almeida, SS, Tonkiss, J, Galler, JR. Prenatal protein malnutrition affects exploratory behavior of female rats in the elevated plus-maze test. Physiol Behav. 1996; 60, 675–680.CrossRefGoogle ScholarPubMed
38. Pare, WP. The performance of WKY rats on three tests of emotional behavior. Physiol Behav. 1992; 51, 1051–1056.CrossRefGoogle ScholarPubMed
39. Pare, WP. Hyponeophagia in Wistar Kyoto (WKY) rats. Physiol Behav. 1994; 55, 975–978.CrossRefGoogle ScholarPubMed
40. Varty, GB, Higgins, GA. Examination of drug-induced and isolation-induced disruptions of prepulse inhibition as models to screen antipsychotic drugs. Psychopharmacology (Berl). 1995; 122, 15–26.CrossRefGoogle ScholarPubMed
41. Lipska, BK, Swerdlow, NR, Geyer, MA, et al. Neonatal excitotoxic hippocampal damage in rats causes post-pubertal changes in prepulse inhibition of startle and its disruption by apomorphine. Psychopharmacology (Berl). 1995; 122, 35–43.CrossRefGoogle ScholarPubMed
42. Swerdlow, NR, Geyer, MA. Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr Bull. 1998; 24, 285–301.CrossRefGoogle Scholar
43. Lane, EA, Albee, GW. The birth weight of children born to schizophrenic women. J Psychol. 1970; 74, 157–160.CrossRefGoogle ScholarPubMed
44. Tashima, L, Nakata, M, Anno, K, Sugino, N, Kato, H. Prenatal influence of ischemia–hypoxia-induced intrauterine growth retardation on brain development and behavioral activity in rats. Biol Neonate. 2001; 80, 81–87.CrossRefGoogle ScholarPubMed
45. Colvin, GB, Sawyer, CH. Induction of running activity by intracerebral implants of estrogen in overiectomized rats. Neuroendocrinology. 1969; 4, 309–320.CrossRefGoogle ScholarPubMed
46. Li, JS, Huang, YC. Early androgen treatment influences the pattern and amount of locomotion activity differently and sexually differentially in an animal model of ADHD. Behav Brain Res. 2006; 175, 176–182.CrossRefGoogle Scholar
47. Morley, JE, Kaiser, FE, Sih, R, Hajjar, R, Perry, HM III. Testosterone and frailty. Clin Geriatr Med. 1997; 13, 685–695.CrossRefGoogle ScholarPubMed
48. Packard, MG, Teather, LA. Intra-hippocampal estradiol infusion enhances memory in ovariectomized rats. Neuroreport. 1997; 8, 3009–3013.CrossRefGoogle ScholarPubMed
49. Fernandes, C, Gonzalez, MI, Wilson, CA, File, SE. Factor analysis shows that female rat behaviour is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacol Biochem Behav. 1999; 64, 731–738.CrossRefGoogle ScholarPubMed
50. Molinari, M, Leggio, MG, Thaut, MH. The cerebellum and neural networks for rhythmic sensorimotor synchronization in the human brain. Cerebellum. 2007; 6, 18–23.CrossRefGoogle ScholarPubMed