Skip to main content Accessibility help
×
Home

Effects of prenatal alcohol exposure on hippocampal volume, verbal learning, and verbal and spatial recall in late childhood

  • KAREN A. WILLOUGHBY (a1) (a2), ERIN D. SHEARD (a1), KELLY NASH (a1) (a3) and JOANNE ROVET (a1) (a2) (a4)

Abstract

Children with prenatal alcohol exposure (PAE) show deficits in verbal learning and spatial memory, as well as abnormal hippocampal development. The relationship between their memory and neuroanatomic impairments, however, has not been directly explored. Given that the hippocampus is integral for the synthesis and retrieval of learned information and is particularly vulnerable to the teratogenic effects of alcohol, we assessed whether reduced learning and recall abilities in children with fetal alcohol spectrum disorders (FASDs) are associated with abnormal hippocampal volumes. Nineteen children with FASDs and 18 typically developing controls aged 9 to 15 years were assessed for verbal learning and verbal and spatial recall and underwent structural magnetic resonance imaging. Images were analyzed for total intracranial volume and for right and left hippocampal volumes. Results revealed smaller left hippocampi and poorer verbal learning and verbal and spatial recall performance in children with FASDs than controls, as well as positive correlations between selective memory indices and hippocampal volumes only in the FASD group. Additionally, hippocampal volumes increased significantly with age in controls only, suggesting that PAE may be associated with long-term abnormalities in hippocampal development that may contribute to impaired verbal learning and verbal and spatial recall. (JINS, 2008, 14, 1022–1033.)

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Effects of prenatal alcohol exposure on hippocampal volume, verbal learning, and verbal and spatial recall in late childhood
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Effects of prenatal alcohol exposure on hippocampal volume, verbal learning, and verbal and spatial recall in late childhood
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Effects of prenatal alcohol exposure on hippocampal volume, verbal learning, and verbal and spatial recall in late childhood
      Available formats
      ×

Copyright

Corresponding author

Correspondence and reprint requests to: Joanne Rovet, Department of Psychology, Rovet Lab, The Hospital for Sick Children, 555 University Avenue, Toronto, ON, Canada. E-mail: joanne.rovet@sickkids.ca

References

Hide All
Abel, E.L. & Sokol, R.J. (1991). A revised conservative estimate of the incidence of FAS and its economic impact. Alcoholism: Clinical and Experimental Research, 15, 514524.
Archibald, S.L., Fennema-Notestine, C., Gamst, A., Riley, E.P., Mattson, S.N., & Jernigan, T.L. (2001). Brain dysmorphology in individuals with severe prenatal alcohol exposure. Developmental Medicine & Child Neurology, 43, 148154.
Autti-Rämö, I., Autti, T., Korkman, M., Kettunen, S., Salonen, O., & Valanne, L. (2002). MRI findings in children with school problems who had been exposed prenatally to alcohol. Developmental Medicine and Child Neurology, 44, 98106.
Benes, F.M., Turtle, M., Khan, Y., & Farol, P. (1994). Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Archives of General Psychiatry, 51, 477484.
Berman, R.F. & Hannigan, J.H. (2000). Effects of prenatal alcohol exposure on the hippocampus: Spatial behavior, electrophysiology and neuroanatomy. Hippocampus, 10, 94110.
Bohbot, V.D., Kalina, M., Stepankova, K., Spackova, N., Petrides, M., & Nadel, L. (1998). Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia, 36, 12171238.
Chudley, A.E., Conry, J., Cook, J.L., Loock, C., Rosales, T., & LeBlanc, N. (2005). Fetal alcohol spectrum disorder: Canadian guidelines for diagnosis. Canadian Medical Association Journal, 172, S1S21.
Clarren, S.K. & Smith, D.W. (1978). The fetal alcohol syndrome. New England Journal of Medicine, 298, 10631067.
Cohen, M.J. (1997). Children's Memory Scale Manual. San Antonio, TX: The Psychological Corporation.
Cornish, I.M. (2000). Factor structure of the Everyday Memory Questionnaire. British Journal of Psychology, 91, 427438.
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (1994). California Verbal Learning Test-Children's Version. San Antonio, TX: The Psychological Corporation.
Donders, J. (1999). Performance discrepancies on the California Verbal Learning Test–Children's Version in the standardization sample. Journal of the International Neuropsychological Society, 5, 2631.
Ghaem, O., Mellet, E., Crivello, F., Tzourio, N., Mazoyer, B., Berthoz, A., & Denis, M. (1997). Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. Neuroreport, 8, 739744.
Gianoulakis, C. (1990). Rats exposed prenatally to alcohol exhibit impairment in spatial navigation test. Behavioural Brain Research, 36, 217228.
Giedd, J.N., Vaituzis, A.C., Hamburger, S.D., Lange, N., Rajapakse, J.C., Kaysen, D., Vauss, Y.C., & Rapoport, J.L. (1996). Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4–18 years. The Journal of Comparative Neurology, 366, 223230.
Goodlett, C.R. & Johnson, T.B. (1999). Temporal windows of vulnerability within the third trimester equivalent: Why “knowing when” matters. In Hannigan, J.H., Goodlett, C.R., Spear, L.P., & Spear, N.E. (Eds.), Alcohol and alcoholism: Effects on brain and development (pp. 5991). Mahwah, NJ: L. Earlbaum Associates.
Greenbaum, R., Nulman, I., Rovet, J., & Koren, G. (2002). The Toronto experience in diagnosing alcohol-related neurodevelopmental disorder: A unique profile of deficits and assets. Canadian Journal of Pharmacology, 9, 215225.
Griffiths, S.Y., Sherman, E.M.S., Slick, D.J., Lautzenhiser, A., Westerveld, M., & Zaroff, C.M. (2006). The factor structure of the CVLT-C in pediatric epilepsy. Child Neuropsychology, 12, 191203.
Hardwood, H. (2000). Updating estimates of the economic costs of alcohol abuse in the United States: Estimates, update methods, and data. Report prepared by The Lewin Group for the National Institute on Alcohol Abuse and Alcoholism.
Iqbal, U., Brien, J.F., Banjanin, S., Andrews, M.H., Matthews, S.G., & Reynolds, J.N. (2005). Chronic prenatal ethanol exposure alters glucocorticoid signalling in the hippocampus of the postnatal guinea pig. Journal of Neuroendocrinology, 17, 600608.
Isaacs, E.B., Lucas, A., Chong, W.K., Wood, S.J., Johnson, C.L., Marshall, C., Vargha-Khadem, F., & Gadian, D.G. (2000). Hippocampal volume and everyday memory in children of very low birth weight. Pediatric Research, 47, 713720.
Jones, K.L. & Smith, D.W. (1973). Recognition of the fetal alcohol syndrome in early infancy. Lancet, 2, 9991001.
Klintsova, A.Y., Helfer, J.L, Calizo, L.H., Dong, W.K., Goodlett, C.R., & Greenough, W.T. (2007). Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure. Alcoholism: Clinical and Experimental Research, 31, 20732082.
Kodituwakku, P.W. (2007). Defining the behavioral phenotype in children with fetal alcohol spectrum disorders: A review. Neuroscience and Biobehavioral Reviews, 31, 192201.
Lenroot, R.K. & Giedd, J.N. (2006). Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging. Neuroscience and Biobehavioral Reviews, 30, 718729.
Livy, D., Miller, E.K., Maier, S.E., & West, J.R. (2003). Fetal alcohol exposure and temporal vulnerability: Effects of binge-like alcohol exposure on the developing rat hippocampus. Neurotoxicology & Teratology, 25, 447458.
Maguire, E.A., Burgess, N., Donnett, J.G., Frackowiak, R.S.J, Frith, C.D., & O'Keefe, J. (1998). Knowing where and getting there: A human navigation network. Science, 280, 921924.
Malisza, K.L., Allman, A., Shiloff, D., Jakobson, L., Longstaffe, S., & Chudley, A.E. (2005). Evaluation of spatial working memory function in children and adults with fetal alcohol spectrum disorders: A functional magnetic resonance imaging study. Pediatric Research, 58, 11501157.
Mattson, S.N. & Riley, E.P. (1998). A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcoholism: Clinical and Experimental Research, 22, 279294.
Mattson, S.N., Riley, E.P., Delis, D.C., Stern, C., & Jones, K.L. (1996). Verbal learning and memory in children with fetal alcohol syndrome. Alcoholism: Clinical and Experimental Research, 20, 810816.
Mattson, S.N., Riley, E.P., Gramling, L., Delis, D.C., & Jones, K.L. (1998). Neuropsychological comparison of alcohol-exposed children with or without physical features of fetal alcohol syndrome. Neuropsychology, 12, 146153.
Mattson, S.N. & Roebuck, T.M. (2002). Acquisition and retention of verbal and nonverbal information in children with heavy prenatal alcohol exposure. Alcoholism: Clinical and Experimental Research, 26, 875882
May, P.A., Fiorentino, D., Gossage, J.P., Kalberg, W.O., Hoyme, H.E., Robinson, L.K., Coriale, G., Jones, K.L., del Campo, M., Tarani, L., Romeo, M., Kodituwakku, P.W., Deiana, K., Buckley, D., & Ceccanti, M. (2006). Epidemiology of FASD in a province in Italy: Prevalence and characteristics of children in a random sample of schools. Alcoholism: Clinical and Experimental Research, 30, 15621575.
May, P.A. & Gossage, J.P. (2001). Estimating the prevalence of fetal alcohol syndrome: A summary. Alcohol Research & Health, 25, 159167.
Niccols, A. (2007). Fetal alcohol syndrome and the developing socio-emotional brain. Brain and Cognition, 65, 135142.
O'Hare, E.D., Kan, E., Yoshii, J., Mattson, S.N., Riley, E.P., Thompson, P.M., Toga, A.W., & Sowell, E.R. (2005). Mapping cerebellar vermal morphology and cognitive correlates in prenatal alcohol exposure. Neuroreport, 16, 12851290.
Osterrieth, P. & Rey, A. (1944). Le test de copie d'une figure complex. Archives de Psychologie, 30, 205221.
Rey, A. (1942). L'examen psychologique dans les cas d'encephalopathie traumatique. Archives de Psychologie, 28, 286340.
Riikonen, R.S., Nokelainen, P., Valkonen, K., Kolehmainen, A.I., Kumpulainen, K.I., Könönen, M., Vanninen, R.L., & Kuikka, J.T. (2005). Deep serotonergic and dopaminergic structures in fetal alcoholic syndrome: A study with nor-β-CIT-single-photon emission computed tomography and magnetic resonance imaging volumetry. Biological Psychiatry, 57, 15651572.
Riikonen, R.S., Salonen, I., Partanen, K., & Verho, S. (1999). Brain perfusion SPECT and MRI in fœtal alcohol syndrome. Developmental Medicine & Child Neurology, 41, 652659.
Riley, E.P. & McGee, C.L. (2005). Fetal alcohol spectrum disorders: An overview with emphasis on changes in brain and behavior. Experimental Biology and Medicine, 230, 357365.
Robinson, G.C., Conry, J.L., & Conry, R.F. (1987). Clinical profile and prevalence of fetal alcohol syndrome in an isolated community in British Columbia. Canadian Medical Association Journal, 137, 203207.
Salorio, C.F., Slomine, B.S., Grados, M.A., Vasa, R.A., Christensen, J.R., & Gerring, J.P. (2005). Neuroanatomic correlates of CVLT-C performance following pediatric traumatic brain injury. Journal of the International Neuropsychological Society, 11, 686696.
Sampson, P.D., Streissguth, A.P., Bookstein, F.L., Little, R.E., Clarren, S.K., Dehaene, P., Hanson, J.W., & Graham, J.M. (1997). Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology, 56, 317326.
Sowell, E.R., Lu, L.H., O'Hare, E.D., McCourt, S.T., Mattson, S.N., O'Connor, M.J., & Bookheimer, S.Y. (2007). Functional magnetic resonance imaging of verbal learning in children with heavy prenatal alcohol exposure. Neuroreport, 18, 635639.
Sowell, E.R., Mattson, S.N., Kan, E., Thompson, P.M., Riley, E.P., & Toga, A.W. (2008). Abnormal cortical thickness and brain-behavior correlation patterns in individuals with heavy prenatal alcohol exposure. Cerebral Cortex, 18, 136144.
Sowell, E.R., Mattson, S.N., Thompson, P.M., Jernigan, T.L., Riley, E.P., & Toga, A.W. (2001). Mapping callosal morphology and cognitive correlates: Effects of heavy prenatal alcohol exposure. Neurology, 57, 235244.
Sowell, E.R., Thompson, P.M., Mattson, S.N., Tessner, K.D., Jernigan, T.L., Riley, E.P., & Toga, A.W. (2002a). Regional brain shape abnormalities persist into adolescence after heavy prenatal alcohol exposure. Cerebral Cortex, 12, 856865.
Sowell, E.R., Trauner, D.A., Gamst, A., & Jernigan, T.L. (2002b). Development of cortical and subcortical brain structures in childhood and adolescence: A structural MRI study. Developmental Medicine & Child Neurology, 44, 416.
Spreen, O. & Strauss, E. (1998). A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary. (2nd ed.). New York: Oxford University Press.
Square, D. (1997). Fetal alcohol syndrome epidemic on Manitoba reserve. Canadian Medical Association Journal, 157, 5960.
Stade, B., Ungar, W.J., Stevens, B., Beyene, J., & Koren, G. (2007). Cost of fetal alcohol spectrum disorder in Canada. Canadian Family Physician, 53, 13031304.
Stratton, K., Howe, C., & Battaglia, F. (1996). Fetal Alcohol Syndrome: Diagnosis, Epidemiology, Prevention, and Treatment. Washington, DC: National Academy Press.
Streissguth, A.P., Aase, J.M., Clarren, S.K., Randels, S.P., LaDue, R.A., & Smith, D.F. (1991). Fetal Alcohol Syndrome in adolescents and adults. The Journal of the American Medical Association, 265, 19611967.
Sunderland, A., Harris, J.E., & Baddeley, A.D. (1983). Assessing everyday memory after severe head injury. In Harris, J.E. & Morris, P.E. (Eds.), Everyday memory, actions, and absent-mindedness (pp. 191206). London: Academic Press.
Sutherland, R.J., McDonald, R.J., & Savage, D.D. (2000). Prenatal exposure to moderate levels of ethanol can have long-lasting effects on learning and memory in adult offspring. Psychobiology, 28, 532539.
Suzuki, M., Hagino, H., Nohara, S., Zhou, S., Kawasaki, Y., Takahashi, T., Matsui, M., Seto, H., Ono, T., & Kurachi, M. (2005). Male-specific volume expansion of the human hippocampus during adolescence. Cerebral Cortex, 15, 187193.
Tomlinson, D., Wilce, P., & Bedi, K.S. (1998). Spatial learning ability of rats following differing levels of exposure to alcohol during early postnatal life. Physiology & Behavior, 63, 205211.
Uecker, A. & Nadel, L. (1996). Spatial locations gone awry: Object and spatial memory deficits in children with fetal alcohol syndrome. Neuropsychologia, 34, 209223.
Van Petten, C. (2004). Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: Review and meta-analysis. Neuropsychologia, 42, 13941413.
Vargha-Khadem, F., Gadian, D.G., Watkins, K.E., Connelly, A., Van Paesschen, W., & Mishkin, M. (1997). Differential effects of early hippocampal pathology on episodic and semantic memory. Science, 277, 376380.
Viljoen, D.L., Gossage, J.P., Brooke, L., Adnams, C.M., Jones, K.L., Robinson, L.K., Hoyme, H.E., Snell, C., Khaole, N.C., Kodituwakku, P., Asante, K.O., Findlay, R., Quinton, B., Marais, A.S., Kalberg, W.O., & May, P.A. (2005). Fetal alcohol syndrome epidemiology in a South African community: A second study of a very high prevalence area. Journal of Studies on Alcohol, 66, 593604.
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. New York: Psychological Corporation.
Willford, J.A., Richardson, G.A., Leech, S.L., & Day, N.L. (2004). Verbal and visuospatial learning and memory function in children with moderate prenatal alcohol exposure. Alcoholism: Clinical and Experimental Research, 28, 497507.
Zhang, X., Sliwowska, J.H., & Weinberg, J. (2005). Prenatal alcohol exposure and fetal programming: Effects on neuroendocrine and immune function. Experimental Biology and Medicine, 230, 376388.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed