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The influence of prenatal experience on behavioral and social development: The benefits and limitations of an animal model

Published online by Cambridge University Press:  02 August 2018

Robert Lickliter*
Affiliation:
Florida International University
*
Address correspondence and reprint requests to: Robert Lickliter, Department of Psychology, Florida International University, Miami, FL 33176; E-mail: licklite@fiu.edu.

Abstract

Prenatal experience is both a formative and a regulatory force in the process of development. As a result, birth is not an adequate starting point for explanations of behavioral development. However, surprisingly little is currently known regarding the role of prenatal experience in the emergence and facilitation of perceptual, cognitive, or social development. Our lack of knowledge in this area is due in part to the very restricted experimental manipulations possible with human fetuses. A comparative approach utilizing animal models provides an essential step in addressing this gap in our knowledge and providing testable predictions for studies with human fetuses, infants, and children. Further, animal-based comparative research serves to minimize the amount of exploratory research undertaken with human subjects and hone in on issues and research directions worthy of further research investment. In this article, I review selected animal-based research exploring how developmental influences during the prenatal period can guide and constrain subsequent behavioral and social development. I then discuss the importance of linking the prenatal environment to postnatal outcomes in terms of how psychologists conceptualize “innate” biases, preferences, and skills in the study of human development.

Type
Special Issue Articles
Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

The writing of this article was supported in part by National Science Foundation Grant BCS 1525371.

References

Alberts, J. R. (1984). Sensory-perceptual development in the Norway rat: A view toward comparative studies. In Kail, R. V. & Spear, N. E. (Eds.), Comparative perspectives on the development of memory (pp. 65102). Hillsdale, NJ: Erlbaum.Google Scholar
Ambrose, A. (1968). The comparative approach to early child development: The data of ethology. In Miller, E. (Ed.), Foundations of child psychiatry (pp. 183232). New York: Pergamon Press.Google Scholar
Arnold, H. M., & Spear, N. E. (1997). Infantile amnesia: Using an animal model to understand forgetting. Advances in the Study of Behavior, 26, 251284.Google Scholar
Bahrick, L. E., & Lickliter, R. (2000). Intersensory redundancy guides attentional selectivity and perceptual learning in infancy. Developmental Psychology, 36, 190201. doi.10.1037/0012-1649.36.2.190Google Scholar
Bahrick, L. E., & Lickliter, R. (2002). Intersensory redundancy guides early perceptual and cognitive development. In Kail, R. (Ed.), Advances in child development and behavior (Vol. 30, pp. 154187). New York: Academic Press.Google Scholar
Bahrick, L. E., & Lickliter, R. (2012). The role of intersensory redundancy in early perceptual, cognitive, and social development. In Bremner, A., Lewkowicz, D. J., & Spence, C. (Eds.), Multisensory development (pp. 183206). New York: Oxford University Press.Google Scholar
Balas, B. (2010). Using innate visual biases to guide face learning in natural scenes: A computational investigation. Developmental Science, 13, 469478. doi:10.1111/j.1467-7687.2009.00901.xGoogle Scholar
Belnap, S., Valesquez, P., & Lickliter, R. (2018). Early social development in bobwhite quail neonates: Exploring the role of intersensory redundancy with robotic quail hens. Unpublished manuscript.Google Scholar
Belzung, C., & Lemoine, M. (2011). Criteria of validity for animal models of psychiatric disorders: Focus on anxiety disorders and depression. Biology of Mood & Anxiety Disorders, 1, 923. doi:10.1186/2045-5380-1-9Google Scholar
Bertin, A., Arnould, C., Mousu, C., Meurisse, M., & Calandreau, L. (2015). Artificially increased yolk hormone levels and neophobia in domestic chicks. Animals, 5. doi:1120-1232.10.3390/ani5040408Google Scholar
Bertin, A., Richard-Yris, M. A., Mostl, E., & Lickliter, R. (2009). Increased yolk testosterone facilitates prenatal perceptual learning in Northern bobwhite quail. Hormones and Behavior, 56, 416422. doi:10.1016/j.yhbeh.2009.07.008Google Scholar
Carlsen, R. M., & Lickliter, R. (1999). Augmented prenatal tactile and vestibular stimulation alters postnatal auditory and visual responsiveness in bobwhite quail chicks. Developmental Psychobiology, 35, 215225.Google Scholar
Casey, M. B., & Sleigh, M. J. (2001). Cross-species investigations of prenatal experience, hatching behavior, and postnatal behavioral laterality. Developmental Psychobiology, 39, 8491. doi:10.1002/dev.1032Google Scholar
Casey, M. B., & Sleigh, M. J. (2014). Prenatal visual experience induces postnatal motor laterality in Japanese quail chicks. Developmental Psychobiology, 56, 489497. doi:10.1002/dev.21116Google Scholar
Curley, J. P., Jensen, C. L., Mashoodh, R., & Champagne, F. A. (2011). Social influences on neurobiology and behavior: Epigenetic effects during development. Psychoneuroendocrinology, 36, 352371. doi:10.1016/j.psyneuen.2010.06.005Google Scholar
Daisley, J. N., Bromundt, V., Mostl, E., & Kotrschal, K. (2005). Enhanced yolk testosterone influences behavioral phenotype independent of sex in Japanese quail chicks. Hormones and Behavior, 47, 185194. doi:10.1016/j.yhbeh.2004.09.006Google Scholar
DeCasper, A., & Fifer, W. P. (1980). Of human bonding: Newborns prefer their mothers’ voices. Science, 208, 11741176. doi:10.1126/science.7375928Google Scholar
DiPietro, J. A. (2010). Maternal influences on the developing fetus. In Zimmerman, A. W. & Conners, S. L. (Eds.), Maternal influences on fetal neurodevelopment: Clinical and research aspects (pp. 1932). New York: Springer.Google Scholar
Emberson, L. L., Boldin, A., Riccio, J. E., Guillet, R., & Aslin, R. N. (2017). Deficits in top down sensory prediction in infants at-risk due to premature birth. Current Biology, 27, 431436. doi:10.1016/j.cub.2016.12.028Google Scholar
Fifer, W. P., & Moon, C. (1995). The effects of fetal experience with sound. In Lecanuet, J. P., Fifer, W. P., Krasnegor, N. A., & Smotherman, W. P. (Eds.), Fetal development: A psychobiological perspective (pp. 351366). Hillsdale, NJ: Erlbaum.Google Scholar
Freeman, B. M., & Vince, M. A. (1974). Development of the avian embryo. London: Chapman and Hall.Google Scholar
Gil, D. (2003). Golden eggs: Maternal manipulation of offspring phenotype by egg androgens in birds. Ardeola, 50, 281294.Google Scholar
Gil, D. (2008). Hormones in avian eggs: Physiology, ecology, and behavior. Advances in the Study of Behavior, 38, 337398. doi:10.1016/S0065-3454(08)00007-7Google Scholar
Gil, D., & Faure, J. M. (2007). Correlated response in yolk testosterone levels following divergent genetic selection for social behavior in Japanese quail. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 307, 9194. doi.10.1002/jez.a.340Google Scholar
Gottlieb, G. (1971a). Development of species identification in birds. Chicago: University of Chicago Press.Google Scholar
Gottlieb, G. (1971b). Ontogenesis of sensory function in birds and mammals. In Tobach, E., Aronson, L. R., & Shaw, E. (Eds.), The biopsychology of development (pp. 67128). New York: Academic Press.Google Scholar
Gottlieb, G. (1997). Synthesizing nature-nurture: Prenatal origins of instinctive behavior. Mahwah, NJ: Erlbaum.Google Scholar
Gottlieb, G., & Lickliter, R. (2004). The various roles of animal models in understanding human development. Social Development, 13, 311325. doi:10.1111/j.1467-9507.2004.000269.xGoogle Scholar
Gottlieb, G., Wahlsten, D., & Lickliter, R. (2006). The significance of biology for human development. In Lerner, R. (Ed.), Handbook of child psychology: Vol. 1. Theoretical models of human development (pp. 210257). New York: Wiley.Google Scholar
Graff, J., Kim, D., Dobbin, M. M., & Tsai, L. H. (2011). Epigenetic regulation of gene expression in physiological and pathological brain processes. Physiological Reviews, 91, 603649. doi:10.1152/physrev.00012.2010Google Scholar
Groothuis, T. G., Muller, W., von Engelhardt, N., Carere, C., & Eising, C. (2005). Maternal hormones as a tool to adjust offspring phenotype in avian species. Neuroscience and Biobehavioral Reviews, 29, 329352. doi:10.1016/j.neubiorev.2004.12.002Google Scholar
Groothuis, T. G., & von Engelhardt, N. (2005). Investigating maternal hormones in avian eggs: Measurement, manipulation, and interpretation. Annals of the New York Academy of Sciences, 1046, 168180. doi:10.1196/annals.1343.014Google Scholar
Haley, D. W., Grunau, R. E., Oberlander, T., & Weinberg, J. (2008). Contingency learning and reactivity in preterm and full-term infants at 3 months. Infancy, 13, 570595. doi:10.1080/15250000802458682Google Scholar
Haley, D. W., Weinberg, J., & Grunau, R. E. (2006). Cortisol, contingency learning, and memory in preterm and full-term infants. Psychoendocrinology, 31, 108117. doi:10.1016/j.psyneuen.2005.06.007Google Scholar
Harshaw, C., & Lickliter, R. (2011). Biased embryos: Prenatal experience and the malleability of species-typical auditory preferences. Developmental Psychobiology, 53, 291302. doi:10.1002/dev.20521Google Scholar
Heaton, M., Miller, D. B., & Goodwin, D. (1978). Species-specific auditory discrimination in bobwhite quail neonates. Developmental Psychobiology, 11, 1321. doi:10.1002/dev.420120112Google Scholar
Herrington, J., Vallin, C., & Lickliter, R. (2015). Increased yolk progesterone elevates emotional reactivity and interferes with prenatal auditory learning in bobwhite quail (Colinus virginianus) chicks. Developmental Psychobiology, 57, 255262. doi:10.1002/dev.21274Google Scholar
Honeycutt, H., & Lickliter, R. (2001). Order-dependent timing of unimodal and multimodal stimulation affects prenatal auditory learning in bobwhite quail embryos. Developmental Psychobiology, 38, 110. doi:10.1002/1098-2302(2001Google Scholar
Honeycutt, H., & Lickliter, R. (2003). The influence of prenatal tactile and vestibular stimulation on auditory and visual responsiveness in bobwhite quail: A matter of timing. Developmental Psychobiology, 43, 7181. doi:10.1002/dev.10122Google Scholar
Hood, K. E., & Cairns, R. B. (1989). The developmental-genetic analysis of aggressive behavior in mice: IV. Genotype-environment interaction. Aggressive Behavior, 15, 361380. doi:10.1007/BF01082312Google Scholar
Jaffe, J., Beebe, B., Feldstein, S., Crown, C. L., & Jasnow, M. D. (2001). Rhythms of dialogue in infancy: Coordinated timing in development. Monographs of the Society for Child Development, 66 (No. 2), pp. 1149.Google Scholar
Jaime, M., & Lickliter, R. (2006). Prenatal exposure to temporal and spatial stimulus properties affects postnatal responsiveness to spatial contiguity in bobwhite quail chicks. Developmental Psychobiology, 48, 233242. doi:10.1002/dev.20131Google Scholar
Jaime, M., Lopez, J. P., & Lickliter, R. (2009). Bobwhite quail neonates track the direction of human gaze. Animal Cognition, 12, 559565. doi:10.1007/s10071-009-0214-3Google Scholar
Kalueff, A. V., & Tuohimaa, P. (2004). Experimental modeling of anxiety and depression. Acta Neurobiologiae Experimentalis, 64, 439448.Google Scholar
Lickliter, R. (1990). Premature visual experience facilitates visual responsiveness in bobwhite quail neonates. Infant Behavior and Development, 13, 487496. doi:10.1016/0163-6383(90)90018-4Google Scholar
Lickliter, R. (1994). Prenatal visual experience alters postnatal sensory dominance hierarchy in bobwhite quail chicks. Infant Behavior and Development, 17, 185193. doi:10.1016/0163-6383(94)90054-XGoogle Scholar
Lickliter, R. (2000). The role of sensory stimulation in perinatal development: Insights from comparative research for the care of the high-risk infant. Journal of Developmental and Behavioral Pediatrics, 21, 437447. doi:10.1097/00004703-200012000-00006Google Scholar
Lickliter, R. (2005). Prenatal sensory ecology and experience: Implications for perceptual and behavioral development in precocial birds. Advances in the Study of Behavior, 35, 235274. doi:10.1016/S0065-3454(05)35006-6Google Scholar
Lickliter, R. (2011). The integrated development of sensory organization. Clinics in Perinatology, 38, 591603. doi:10.1016/j.clp.2011.08.007Google Scholar
Lickliter, R., Bahrick, L. E., & Honeycutt, H. (2002). Intersensory redundancy facilitates prenatal perceptual learning in bobwhite quail embryos. Developmental Psychology, 38, 1523. doi:10.1037/0012-1649.38.1.15Google Scholar
Lickliter, R., Bahrick, L. E., & Honeycutt, H. (2004). Intersensory redundancy enhances memory in bobwhite quail embryos. Infancy, 5, 253269. doi:10.1207/s15327078in0503_1Google Scholar
Lickliter, R., Bahrick, L. E., & Markham, R. (2006). Intersensory redundancy educates selective attention in bobwhite quail embryos. Developmental Science, 9, 604615. doi:10.1111/j.1467-7687.2006.00539.xGoogle Scholar
Lickliter, R., Bahrick, L. E., & Vaillant-Mekras, J. (2017). The intersensory redundancy hypothesis: Extending the principle of unimodal facilitation to prenatal development. Developmental Psychobiology, 59, 910915. doi:10.1002/dev.21551Google Scholar
Markham, R., Shimizu, T., & Lickliter, R. (2008). Extrinsic embryonic sensory stimulation alters multimodal behavior and cellular activation. Developmental Neurobiology, 68, 14631473. doi:10.1002/dneu.20667Google Scholar
Mastropieri, D., & Turkewitz, G. (1999). Prenatal exposure and neonatal responsiveness to vocal expression of emotion. Developmental Psychobiology, 35, 204214. doi:10.1002/(SICI)1098-2302Google Scholar
Meltzoff, A. N., & Decety, J. (2003). What imitation tells us about social cognition: A rapprochement between developmental psychology and cognitive neuroscience. Philosophical Transactions of the Royal Society of London B, 358, 491500. doi:10.1098/rstb.2002.1261Google Scholar
Moon, C., Panneton-Cooper, R., & Fifer, W. P. (1993). Two-day-olds prefer their native language. Infant Behavior and Development, 16, 495500.Google Scholar
Moore, D. S. (2009). Probing predispositions: The pragmatism of a process perspective. Child Development Perspectives, 3, 9193. doi:10.1111/j.1750-8606.2009.00083.xGoogle Scholar
Moore, D. S. (2015). The developing genome: An introduction to behavioral epigenetics. New York: Oxford University Press.Google Scholar
Mueller, B. R., & Bale, T. L. (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience, 28, 90559065. doi:10.1523/jneurosci.1424-08.2008Google Scholar
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. (2008). Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics, 3, 97106. doi:10.4161/epi.3.2.6034Google Scholar
O'Dowd, B. (2014). Effects of prenatal sensory stimulation on perceptual narrowing in bobwhite quail neonates (Unpublished doctoral dissertation, Florida International University).Google Scholar
Oyama, S. (2000). The ontogeny of information: Developmental systems and evolution. Durham, NC: Duke University Press.Google Scholar
Previc, F. (1991). A general theory concerning the prenatal origins of cerebral lateralization in humans. Psychological Review, 98, 299334. doi:10.1037/0033-295X.98.3.299Google Scholar
Radell, P., & Gottlieb, G. (1992). Developmental sensory interference: Augmented prenatal sensory experience interferes with auditory learning in duck embryos. Developmental Psychology, 28, 795803. doi:10.1037/0012-1649.28.5.795Google Scholar
Raju, N. (2014). Effects of prenatal visual stimulation on contingency learning in bobwhite quail neonates (Unpublished doctoral dissertation, Florida International University).Google Scholar
Reynolds, G., & Lickliter, R. (2002). Effects of prenatal sensory stimulation on heart rate and behavioral measures of arousal in bobwhite quail embryos. Developmental Psychobiology, 41, 112122. doi:10.1002/dev.10058Google Scholar
Reynolds, G., & Lickliter, R. (2004). Modified prenatal sensory stimulation influences postnatal behavioral and perceptual responsiveness in bobwhite quail chicks. Journal of Comparative Psychology, 118, 172178. doi:10.1037/0735-7036.118.2.172Google Scholar
Rochat, P. (2001). Social contingency detection and infant development. Bulletin of the Meinninger Clinic, 65, 347361.Google Scholar
Ronca, A. E., & Alberts, J. A. (2016). Fetal and birth experiences: Proximate effects, developmental consequences, epigenetic legacies. In Reissland, N. & Kisilevsky, B. S. (Eds.), Fetal development (pp. 1542). New York: Springer.Google Scholar
Salazar, A. N., & Lickliter, R. (2018). Elevated prenatal testosterone interferes with postnatal gaze tracking in bobwhite quail chicks. Unpublished manuscript.Google Scholar
Schaal, B., Marlier, L., & Soussignan, R. (1998). Neonatal responsiveness to the odor of amniotic and lacteal fluids: A test of perinatal chemosensory continuity. Child Development, 69, 611623. doi:10.1111/j.1467-8624.1998.tb06232.xGoogle Scholar
Schwabl, H. (1993). Yolk as a source of maternal testosterone in developing birds. Proceedings of the National Academy of Science, 90, 1144611450.Google Scholar
Sleigh, M. J., & Lickliter, R. (1998). Timing of the presentation of prenatal auditory stimulation affects postnatal perceptual responsiveness in bobwhite quail chicks. Journal of Comparative Psychology, 112, 153160. doi:10.1037/0735-7036.112.2.153Google Scholar
Smith, G. C., Gutorich, J., Smyser, C., Pineda, R., Newnham, C., Tjoeng, T. H., … Inder, T. E. (2011). Exposure to stressors in the NICU is associated with regional alterations in brain structure and function, including in motor behavior. Annals of Neurology, 70, 541549.Google Scholar
Stoddard, H. L. (1931). The bobwhite quail. New York: Scribner's.Google Scholar
Stokes, A. W. (1967). Behavior of the bobwhite (Colinus virginianus). Auk, 84, 133.Google Scholar
Streri, A., Coulen, M., & Guellai, B. (2013). The foundations of social cognition: Studies of face/voice integration in newborn infants. International Journal of Behavioral Development, 37, 7983. doi:10.1117/0165025412465361Google Scholar
Sultan, F. A., & Day, J. (2011). Epigenetic mechanisms in memory and synaptic function. Epigenomics, 3, 157181. doi:10.2217/epi.11.6Google Scholar
Sweatt, J. D. (2010). Epigenetics and cognitive aging. Science, 328, 701702. doi:10.1126/science.1189968Google Scholar
Tarabulsy, G. M., Tessier, R., & Kappas, A. (1996). Contingency detection and the contingent organization of behavior in interactions: Implications for socioemotional development in infancy. Psychological Bulletin, 120, 2541. doi:10.1037/0033-2909.120.1.25Google Scholar
Taylor, H. G., Minich, N. M., Klein, N., & Hack, M. (2004). Longitudinal outcomes of very low birthweight: Neuropsychological findings. Journal of the International Neuropsychological Society, 10, 149163. doi:10.1017/S1355617704102038Google Scholar
Turkewitz, G., & Kenny, P. A. (1982). Limitations on input as a basis for neural organization and perceptual development: A preliminary theoretical statement. Developmental Psychobiology, 15, 357368. doi:10.1002/dev.420150408Google Scholar
Turkewitz, G., & Mellon, R. C. (1989). Dynamic organization of sensory function. Canadian Journal of Psychology, 43, 286301. doi:10.1037/h0084214Google Scholar
Tusculescu, R. A., & Griswold, J. G. (1983). Prehatching interactions in domestic chicks. Animal Behaviour, 31, 110. doi:10.1016/S0003-3472(83)80168-7Google Scholar
Willner, P. (1984). The validity of animal models of depression. Psychopharmacology, 83, 116. doi:10.1007/BF00427414Google Scholar