Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cb9f654ff-plnhv Total loading time: 0.001 Render date: 2025-08-09T23:09:58.456Z Has data issue: false hasContentIssue false

4 - Sensitive Periods in the Behavioral Development of Mammals

Published online by Cambridge University Press:  26 May 2010

By
Christoph Wiedenmayer
Edited by
Carol M. Worthman ,
Paul M. Plotsky ,
Daniel S. Schechter  and
Constance A. Cummings
Carol M. Worthman
Affiliation:
Emory University, Atlanta
Paul M. Plotsky
Affiliation:
Emory University, Atlanta
Daniel S. Schechter
Affiliation:
Hôpitaux Universitaires de Genève
Constance A. Cummings
Affiliation:
Foundation for Psychocultural Research, California
Get access

Summary

Experience can modify the behavior of animals anytime during their lifespan. Sometimes an experience is so powerful that it can alter the animal's behavior in an enduring way. It has been argued that environmental influences are particularly effective in shaping behavior when they occur in early development. This view implies that early experience differs from experience in adulthood. In other words, there are specific periods during development, windows of susceptibility, when experience has a significantly stronger impact on brain and behavior compared to other periods. In this review, I will try to answer the question, “Do particular periods exist in the early lives of mammals during which experience has long-lasting consequences in brain and behavior?” I will first describe the concept of sensitive periods, and then summarize studies that demonstrate an effect of early experience on later behavior. Examples include olfactory learning about the caregiver and the consequences of aversive stimulation on anxiety and fear. I will discuss the neural bases of experience-dependent changes in behavior during sensitive periods, and suggest, finally, that whereas early experience can result in adaptive adjustments to local environments, it can also lead to disruption and maladaptation.

THE CONCEPT OF SENSITIVE PERIOD

The idea that experience has a more pronounced and a longer lasting effect during early development than later in life has a long history. The ethologist Konrad Lorenz introduced the concept of “critical period” into the behavioral sciences (Lorenz, 1937).

Information

Type
Chapter
Information
Formative Experiences
The Interaction of Caregiving, Culture, and Developmental Psychobiology
 , pp. 82 - 105
Publisher: Cambridge University Press
Print publication year: 2010

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.)

Book purchase

Temporarily unavailable

References

Alcock, J. (2005). Animal Behavior (8th ed.). Sunderland, MA: Sinauer Associates.Google Scholar
Andersen, S. L. (2003). Trajectories of brain development: Point of vulnerability or window of opportunity?Neuroscience and Biobehavioral Reviews, 27, 3–18.CrossRefGoogle ScholarPubMed
Andersen, S. L., & Teicher, M. H. (2008). Stress, sensitive periods and maturational events in adolescent depression. Trends in Neurosciences, 31, 183–191.CrossRefGoogle ScholarPubMed
Andersen, S. L., Tomada, A., Vincow, E. S., Valente, E., Polcari, A., & Teicher, M. H. (2008). Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. Journal of Neuropsychiatry & Clinical Neurosciences, 20, 292–301.CrossRefGoogle ScholarPubMed
Armstrong, C. M., DeVito, L. M., & Cleland, T. A. (2006). One-trial associative odor learning in neonatal mice. Chemical Senses, 31, 343–349.CrossRefGoogle ScholarPubMed
Bachevalier, J., & Vargha-Khadem, F. (2005). The primate hippocampus: Ontogeny, early insult and memory. Current Opinion in Neurobiology, 15, 168–174.CrossRefGoogle ScholarPubMed
Bateson, P. (1978). Sexual imprinting and optimal outbreeding. Nature, 273, 659–660.CrossRefGoogle ScholarPubMed
Bateson, P. (1979). How do sensitive periods arise and what are they for?Animal Behaviour, 27, 470–486.CrossRefGoogle Scholar
Bateson, P. (1990). Is imprinting such a special case?Philosophical Transactions of the Royal Society B., 329, 125–131.CrossRefGoogle Scholar
Bischof, H.-J. (2007). Behavioral and neuronal aspects of developmental sensitive periods. NeuroReport, 18, 461–465.CrossRefGoogle ScholarPubMed
Blais, I., Terkel, J., & Goldblatt, A. (2006). Long-term impact of early olfactory experience on later olfactory conditioning. Developmental Psychobiology, 48, 501–507.CrossRefGoogle ScholarPubMed
Blakemore, S.-J. (2008). The social brain in adolescence. Nature Reviews Neuroscience, 9, 267–277.CrossRefGoogle ScholarPubMed
Bolhuis, J. J., & Honey, R. C. (1998). Imprinting, learning and development: From behaviour to brain and back. Trends in Neurosciences, 21, 306–311.CrossRefGoogle Scholar
Bornstein, M. H. (1989). Sensitive periods in development: Structural characteristics and causal interpretations. Psychological Bulletin, 105, 179–197.CrossRefGoogle ScholarPubMed
Bottjer, S. W. (2002). Neural strategies for learning during sensitive periods of development. Journal of Comparative Physiology A, 188, 917–928.Google ScholarPubMed
Bouslama, M., Durand, E., Chauviere, L., Bergh, O., & Gallego, J. (2005). Olfactory classical conditioning in newborn mice. Behavioral Brain Research, 161, 102–106.CrossRefGoogle ScholarPubMed
Brake, S. C. (1981). Suckling infant rats learn a preference for a novel olfactory stimulus paired with milk delivery. Science, 211, 506–508.CrossRefGoogle Scholar
Brennan, P. A., & Kendrick, K. M. (2006). Mammalian social odours: Attraction and individual recognition. Philosophical Transactions of the Royal Society B, 361, 2061–2078.CrossRefGoogle ScholarPubMed
Broad, K. D., Curley, J. P., & Keverne, E. B. (2006). Mother-infant bonding and the evolution of mammalian social relationships. Philosophical Transactions of the Royal Society B, 361, 2199–2214.CrossRefGoogle ScholarPubMed
Brunelli, S. A., Shair, H. N., & Hofer, M. A. (1994). Hypothermic vocalizations of rat pups (Rattus norvegicus) elicit and direct maternal search behavior. Journal of Comparative Psychology, 108, 298–303.CrossRefGoogle ScholarPubMed
Campbell, B. A., & Spear, N. E. (1972). Ontogeny of memory. Psychological Review, 79, 215–236.CrossRefGoogle Scholar
Carroll, J. C., Boyce-Rustay, J. M., Millstein, R., Yang, R., Wiedholz, L. M., Murphy, D. L., & Holmes, A. (2007). Effects of mild early life stress on abnormal emotion-related behaviors in 5-HTT knockout mice. Behavioral Genetics, 37, 214–222.CrossRefGoogle ScholarPubMed
Carter, C. S., & Marr, J. N. (1970). Olfactory imprinting and age variables in the guinea-pig Cavia porcellus. Animal Behaviour, 18, 238–244.CrossRefGoogle ScholarPubMed
Chen, S. W. C., Shemyakin, A., & Wiedenmayer, C. P. (2006). The role of the amygdala and olfaction in unconditioned fear in developing rats. Journal of Neuroscience, 26, 233–240.CrossRefGoogle ScholarPubMed
Cohen, H., Kaplan, Z., Matar, M. A., Loewenthal, U., Zohar, J., & Richter-Levin, G. (2007). Long-lasting behavioral effects of juvenile trauma in an animal model of PTSD associated with a failure of the autonomic nervous system to recover. European Journal of Neuropsychopharmacology, 17, 464–477.CrossRefGoogle Scholar
Coopersmith, R., & Leon, M. (1984). Enhanced neural response to familiar olfactory cues. Science, 225, 849–851.CrossRefGoogle ScholarPubMed
Coopersmith, R., & Leon, M. (1986). Enhanced neural response by adult rats to odors experienced early in life. Brain Research, 371, 400–403.CrossRefGoogle ScholarPubMed
Coureaud, G., Moncomble, A.-S., Montigny, D., Dewas, M., Perrier, G., & Schaal, B. (2006). A pheromone that rapidly promotes learning in the newborn. Current Biology, 16, 1956–1961.CrossRefGoogle ScholarPubMed
Dawson, G., Ashman, S. B., & Carver, L. J. (2000). The role of early experience in shaping behavioral and brain development and its implications for social policy. Developmental Psychopathology, 12, 695–712.CrossRefGoogle ScholarPubMed
Dumas, T. C. (2005a). Developmental regulation of cognitive abilities: Modified composition of a molecular switch turns on associative learning. Progress in Neurobiology, 76, 189–211.CrossRefGoogle ScholarPubMed
Dumas, T. C. (2005b). Late postnatal maturation of excitatory synaptic transmission permits adult-like expression of hippocampal-dependent behaviors. Hippocampus, 15, 562–578.CrossRefGoogle ScholarPubMed
Fanselow, M. S., & Lester, L. S. (1988). A functional behavioristic approach to aversively motivated behavior: Predatory imminence as a determinant of the topography of defensive behavior. In Bolles, R. C. & Beecher, M. D. (Eds.), Evolution and Learning (pp. 185–212). Hillsdale, NJ: Lawrence Erlbaum.Google Scholar
Fillion, T. J., & Blass, E. M. (1986). Infantile experience with suckling odors determines adult sexual behavior in male rats. Science, 231, 729–731.CrossRefGoogle ScholarPubMed
Franks, K. M., & Isaacson, J. S. (2005). Synapse-specific downregulation of NMDA receptors by early experience: A critical period for plasticity of sensory input to olfactory cortex. Neuron, 47, 101–114.CrossRefGoogle ScholarPubMed
Gale, G. D., Anagnostaras, S. G., Godsil, B. P., Mitchell, S., Nozawa, T., Sage, J. R., et al. (2004). Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. Journal of Neuroscience, 24, 3810–3815.CrossRefGoogle ScholarPubMed
Gaspar, P., Cases, O., & Maroteaux, L. (2003). The developmental role of serotonin: News from mouse molecular genetics. Nature Reviews Neuroscience, 4, 1002–1012.CrossRefGoogle ScholarPubMed
Griffin, A. S. (2004). Social learning about predators: A review and prospectus. Learning & Behavior, 32, 131–140.CrossRefGoogle ScholarPubMed
Gross, C., Zhuang, X., Stark, K., Ramboz, S., Oosting, R., Kirby, L., et al. (2002). Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature, 416, 396–400.CrossRefGoogle ScholarPubMed
Hayne, H. (2004). Infant memory development: Implications for childhood amnesia. Developmental Review, 24, 33–73.CrossRefGoogle Scholar
Heim, C., & Nemeroff, C. B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biological Psychiatry, 49, 1023–1039.CrossRefGoogle ScholarPubMed
Hensch, T. K. (2004). Critical period regulation. Annual Review of Neuroscience, 27, 549–579.CrossRefGoogle ScholarPubMed
Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nature Reviews Neuroscience, 6, 877–888.CrossRefGoogle ScholarPubMed
Hepper, P. G. (1986). Parental recognition in the rat. Quarterly Journal of Experimental Psychology, 38B, 151–160.Google Scholar
Hepper, P. G. (1994). Long-term retention of kinship recognition established during infancy in the domestic dog. Behavioral Processes, 33, 3–14.CrossRefGoogle ScholarPubMed
Hepper, P. G., & Cleland, J. (1999). Developmental aspects of kin recognition. Genetica, 104, 199–205.CrossRefGoogle Scholar
Herlenius, E., & Lagercrantz, H. (2004). Development of neurotransmitter systems during critical periods. Experimental Neurology, 190, S8–S21.CrossRefGoogle ScholarPubMed
Hofer, M. A. (1994). Hidden regulators in attachment, separation, and loss. Monographs of the Society for Research in Child Development, 59, 192–207.CrossRefGoogle ScholarPubMed
Hofer, M. A. (2005). The psychobiology of early attachment. Clinical Neuroscience Research, 4, 291–300.CrossRefGoogle Scholar
Hofer, M. A., & Shair, H. (1978). Ultrasonic vocalization during social interaction and isolation in 2-week-old rats. Developmental Psychobiology, 11, 495–504.CrossRefGoogle Scholar
Hofer, M. A., Shair, H., & Singh, P. (1976). Evidence that maternal ventral skin substances promote suckling in infant rats. Physiology & Behavior, 17, 131–136.CrossRefGoogle ScholarPubMed
Horn, G. (1998). Visual imprinting and the neural mechanisms of recognition memory. Trends in Neurosciences, 21, 300–305.CrossRefGoogle ScholarPubMed
Hudson, R. (1985). Do newborn rabbits learn the odor stimuli releasing nipple-search behavior?Developmental Psychobiology, 18, 575–585.CrossRefGoogle ScholarPubMed
Hudson, R. (1993). Olfactory imprinting. Current Opinion in Neurobiology, 3, 548–552.CrossRefGoogle ScholarPubMed
Johnson, B. A., Woo, C. C., Duong, H., Nguyen, V., & Leon, M. (1995). A learned odor evokes an enhanced Fos-like glomerular response in the olfactory bulb of young rats. Brain Research, 699, 192–200.CrossRefGoogle ScholarPubMed
Johnson, M. H. (2005). Sensitive periods in functional brain development: Problems and prospects. Developmental Psychobiology, 46, 287–292.CrossRefGoogle ScholarPubMed
Katz, L. C., & Shatz, C. J. (1996). Synaptic activity and the construction of cortical circuits. Science, 274, 1133–1138.CrossRefGoogle ScholarPubMed
Kendler, K. S., Kuhn, J. W., & Prescott, C. A. (2004). Childhood sexual abuse, stressful life events and risk for major depression in women. Psychological Medicine, 34, 1475–1482.CrossRefGoogle ScholarPubMed
Kendrick, K. M., Hinton, M. R., Atkins, K., Haupt, M. A., & Skinner, J. D. (1998). Mothers determine sexual preferences. Nature, 395, 229–230.CrossRefGoogle ScholarPubMed
Kim, J. H., McNally, G. P., & Richardson, R. (2006). Recovery of fear memories in rats: Role of gamma-amino butyric acid (GABA) in infantile amnesia. Behavioral Neuroscience, 120, 40–48.CrossRefGoogle Scholar
Kindermann, U., Hudson, R., & Distel, H. (1994). Learning of suckling odors by newborn rabbits declines with age and suckling experience. Developmental Psychobiology, 27, 111–122.CrossRefGoogle ScholarPubMed
Knudsen, E. I. (2004). Sensitive periods in the development of the brain and behavior. Journal of Cognitive Neuroscience, 16, 1412–1425.CrossRefGoogle ScholarPubMed
Konno, K., Matsumoto, M., Togashi, H., Yamaguchi, T., Izumi, T., Watanabe, M., et al. (2007). Early postnatal stress affects the serotonergic function in the median raphe nuclei of adult rats. Brain Research, 1172, 60–66.CrossRefGoogle ScholarPubMed
Lamprecht, R., & LeDoux, J. E. (2004). Structural plasticity and memory. Nature Reviews Neuroscience, 5, 45–54.CrossRefGoogle ScholarPubMed
Leon, M. (1992). Neuroethology of olfactory preference development. Journal of Neurobiology, 23, 1557–1573.CrossRefGoogle ScholarPubMed
Leonardo, E. D., & Hen, R. (2008). Anxiety as a developmental disorder. Neuropsychopharmacology, 33, 134–140.CrossRefGoogle ScholarPubMed
Levine, S. (2001). Primary social relationships influence the development of the hypothalamic-pituitary-adrenal axis in the rat. Physiology & Behavior, 73, 255–260.CrossRefGoogle ScholarPubMed
Lima, S. L., & Dill, L. M. (1990). Behavioral decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology, 68, 619–640.CrossRefGoogle Scholar
Lind, J., & Cresswell, W. (2005). Determining the fitness consequences of antipredation behavior. Behavioral Ecology, 16, 945–956.CrossRefGoogle Scholar
Lo Iacono, L., & Gross, C. (2008). α-Ca2+/calmodulin-dependent protein kinase II contributes to the developmental programming of anxiety in serotonin receptor 1A knock-out mice. Journal of Neuroscience, 28, 6250–6257.CrossRefGoogle ScholarPubMed
Lorenz, K. Z. (1937). The companion in the bird's world. The Auk, 54, 245–273.CrossRefGoogle Scholar
Mateo, J. M. (1996). The development of alarm-call response behaviour in free-living juvenile Belding's ground squirrels. Animal Behaviour, 52, 489–505.CrossRefGoogle Scholar
Matsumoto, M., Higuchi, K., Togashi, H., Koseki, H., Yamaguchi, T., Kanno, M., et al. (2005). Early postnatal stress alters the 5-HTergic modulation to emotional stress at postadolescent periods of rats. Hippocampus, 15, 775–781.CrossRefGoogle ScholarPubMed
McLean, J. H., & Harley, C. W. (2004). Olfactory learning in the rat pup: A model that may permit visualization of a mammalian memory trace. NeuroReport, 15, 1691–1697.CrossRefGoogle ScholarPubMed
Michel, G. F., & Tyler, A. N. (2005). Critical period: A history of the transition from questions of when, to what, to how. Developmental Psychobiology, 46, 156–162.CrossRefGoogle Scholar
Mineka, S., Davidson, M., Cook, M., & Keir, R. (1984). Observational conditioning of snake fear in rhesus monkeys. Journal of Abnormal Psychology, 93, 355–372.CrossRefGoogle ScholarPubMed
Mizuno, K., Mizuno, N., Shinohara, T., & Noda, M. (2004). Mother-infant skin-to-skin contact after delivery results in early recognition of own mother's milk odour. Acta Paediatrica, 93, 1640–1645.CrossRefGoogle ScholarPubMed
Moriceau, S., & Sullivan, R. M. (2004). Unique neural circuitry for neonatal olfactory learning. Journal of Neuroscience, 24, 1182–1189.CrossRefGoogle ScholarPubMed
Moriceau, S., & Sullivan, R. M. (2005). Neurobiology of infant attachment. Developmental Psychobiology, 47, 230–242.CrossRefGoogle ScholarPubMed
Moriceau, S., Wilson, D. A., Levine, S., & Sullivan, R. M. (2006). Dual circuitry for odor-shock conditioning during infancy: Corticosterone switches between fear and attraction via amygdala. Journal of Neuroscience, 26, 6737–6748.CrossRefGoogle ScholarPubMed
Owings, D. H., & Coss, R. G. (1977). Snake mobbing by California ground squirrels: Adaptive variation and ontogeny. Behaviour, 62, 50–69.CrossRefGoogle Scholar
Parks, C. L., Robinson, P. S., Sibille, E., Shenk, T., & Toth, M. (1998). Increased anxiety of mice lacking the serotonin1A receptor. Proceedings of the National Academy of Sciences of the United States of America, 95, 10734–10739.CrossRefGoogle ScholarPubMed
Penn, D., & Potts, W. (1998). MHC-disassortative mating preferences reversed by cross-fostering. Proceedings of the Royal Society of London B, 265, 1299–1306.CrossRefGoogle ScholarPubMed
Penn, D. J. (2002). The scent of genetic compatibility: Sexual selection and the major histocompatibility complex. Ethology, 108, 1–21.CrossRefGoogle Scholar
Pentkowski, N. S., Blanchard, D. C., Lever, C., Litvin, Y., & Blanchard, R. J. (2006). Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. European Journal of Neuroscience, 23, 2185–2196.CrossRefGoogle ScholarPubMed
Pillemer, D. B. (1998). What is remembered about early childhood events?Clinical Psychology Review, 18, 895–913.CrossRefGoogle ScholarPubMed
Polan, H. J., Milano, D., Eljuga, L., & Hofer, M. A. (2002). Development of rats' maternally directed orienting behaviors from birth to day 2. Developmental Psychobiology, 40, 81–103.CrossRefGoogle ScholarPubMed
Poo, C., & Isaacson, J. S. (2007). An early critical period for long-term plasticity and structural modification of sensory synapses in olfcatory cortex. Journal of Neuroscience, 27, 7553–7558.CrossRefGoogle Scholar
Ramboz, S., Oosting, R., Amara, D. A., Kung, H. F., Blier, P., Mendelsohn, M., et al. (1998). Serotonin receptor 1A knockout: An animal model of anxiety-related disorder. Proceedings of the National Academy of Sciences of the United States of America, 95, 14476–14481.CrossRefGoogle ScholarPubMed
Rodriguez Echandia, E. L., Foscolo, M., & Broitman, S. T. (1982). Preferential nesting in lemon-scented environment in rats reared on lemon-scented bedding from birth to weaning. Physiology & Behavior. Behav., 29, 47–49.CrossRefGoogle ScholarPubMed
Romantshik, O., Porter, R. H., Tillmann, V., & Varendi, H. (2007). Preliminary evidence of a sensitive period for olfactory learning by human newborns. Acta Paediatrica, 96, 372–376.CrossRefGoogle ScholarPubMed
Roth, T. L., & Sullivan, R. M. (2005). Memory of early maltreatment: Neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning. Biological Psychiatry, 57, 823–831.CrossRefGoogle ScholarPubMed
Rudy, J. W. (1991). Elemental and configural associations, the hippocampus and development. Developmental Psychobiology, 24, 221–236.CrossRefGoogle Scholar
Schaal, B., Coureaud, G., Langlois, D., Giniès, C., Sémon, E., & Perrier, G. (2003). Chemical and behavioural characterization of the rabbit mammary pheromone. Nature, 424, 68–72.CrossRefGoogle ScholarPubMed
Sevelinges, Y., Moriceau, S., Holman, P., Miner, C., Muzny, K., Gervais, R., Mouly, A.-M., & Sullivan, R. M. (2007). Enduring effects of infant memories: Infant odor-shock conditioning attenuates amygdala activity and adult fear conditioning. Biological Psychiatry, 62, 1070–1079.CrossRefGoogle ScholarPubMed
Shah, A., Oxley, G., Lovic, V., & Fleming, A. S. (2002). Effects of preweaning exposure to novel maternal odors on maternal responsiveness and selectivity in adulthood. Developmental Psychobiology, 41, 187–196.CrossRefGoogle ScholarPubMed
Shier, D. M., & Owings, D. H. (2007). Effects of social learning on predator training and postrelease survival in juvenile black-tailed prairie dogs, Cynomys ludovicianus. Animal Behaviour, 73, 567–577.CrossRefGoogle Scholar
Singh, P. J., Tucker, A. M., & Hofer, M. A. (1976). Effects of nasal ZnSO4 irrigation and olfactory bulbectomy on rat pups. Physiology & Behavior, 17, 373–382.CrossRefGoogle ScholarPubMed
Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417–463.CrossRefGoogle ScholarPubMed
Sullivan, R. M. (2003). Developing a sense of safety: The neurobiology of neonatal attachment. Annual New York Academy of Sciences, 1008, 122–131.CrossRefGoogle ScholarPubMed
Sullivan, R. M., Hofer, M. A., & Brake, S. C. (1986). Olfactory-guided orientation in neonatal rats is enhanced by a conditioned change in behavioral state. Developmental Psychobiology, 19, 615–623.CrossRefGoogle ScholarPubMed
Sullivan, R. M., Landers, M., Yeaman, B., & Wilson, D. A. (2000). Good memories of bad events in infancy. Nature, 407, 38–39.CrossRefGoogle ScholarPubMed
Sullivan, R. M., & Leon, M. (1987). One-trial olfactory learning enhances olfactory bulb responses to an appetitive conditioned odor in 7-day-old rats. Developmental Brain Research, 35, 307–311.CrossRefGoogle Scholar
Sullivan, R. M., & Wilson, D. A. (1994). The locus coeruleus, norepinephrine, and memory in newborns. Brain Research Bulletin, 35, 467–472.CrossRefGoogle ScholarPubMed
Sullivan, R. M., Wilson, D. A., & Leon, M. (1989). Norepinephrine and learning-induced plasticity in infant rat olfactory system. Journal of Neuroscience, 9, 3998–4006.CrossRefGoogle ScholarPubMed
Takahashi, L. K. (1992). Developmental expression of defensive responses during exposure to conspecific adults in preweanling rats (Rattus norvegicus). Journal of Comparative Psychology, 106, 69–77.CrossRefGoogle Scholar
Takahashi, L. K. (1995). Glucocorticoids, the hippocampus, and behavioral inhibition in the preweanling rat. Journal of Neuroscience, 15, 6023–6034.CrossRefGoogle ScholarPubMed
Tanapat, P., Galea, L. A. M., & Gould, E. (1998). Stress inhibits the proliferation of granule cell percursors in the developing dentate gyrus. International Journal of Developmental Neuroscience, 16, 235–239.CrossRefGoogle Scholar
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., Navalta, C. P., & Kim, D. M. (2003). The neurobiological consequences of early stress and childhood maltreatment. Neuroscience and Biobehavioral Reviews, 27, 33–44.CrossRefGoogle ScholarPubMed
Teicher, M. H., & Blass, E. M. (1977). First suckling response of the newborn albino rat: The roles of olfaction and amniotic fluid. Science, 198, 635–636.CrossRefGoogle ScholarPubMed
Thompson, J. V., Sullivan, R. M., & Wilson, D. A. (2008). Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity. Brain Research, 1200, 58–65.CrossRefGoogle ScholarPubMed
Tsoory, M., Cohen, H., & Richter-Levin, G. (2007). Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood. European Neuropsychopharmacology, 17, 245–256.CrossRefGoogle ScholarPubMed
Varendi, H., Porter, R. H., & Winberg, J. (1994). Does the newborn baby find the nipple by smell?Lancet, 344, 989–990.CrossRefGoogle ScholarPubMed
Vidal, J., de Bie, J., Granneman, R. A., Wallinga, A. E., Koolhaas, J. M., & Buwalda, B. (2007). Social stress during adolescence in Wistar rats induces social anxiety in adulthood without affecting brain monoaminergic content and activity. Physiology & Behavior, 92, 824–830.CrossRefGoogle ScholarPubMed
Wiedenmayer, C. P. (2004). Adaptations or pathologies? Long-term changes in brain and behavior after a single exposure to severe threat. Neuroscience and Biobehavioral Reviews, 28, 1–12.CrossRefGoogle ScholarPubMed
Wiedenmayer, C. P., & Barr, G. A. (2001). Developmental changes in responsivity to threat are stimulus-specific in rats. Developmental Psychobiology, 39, 1–7.CrossRefGoogle ScholarPubMed
Wiedenmayer, C. P., Lyo, D., & Barr, G. A. (2003). Rat pups reduce ultrasonic vocalization after exposure to an adult male rat. Developmental Psychobiology, 42, 386–391.CrossRefGoogle Scholar
Wiesel, T. N., & Hubel, D. H. (1963). Single-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology, 26, 1003–1017.CrossRefGoogle ScholarPubMed
Wilson, D. A., Pham, T.-C., & Sullivan, R. M. (1994). Norepinephrine and posttraining memory consolidation in neonatal rats. Behavioral Neuroscience, 108, 1053–1058.CrossRefGoogle ScholarPubMed
Wilson, D. A., & Sullivan, R. M. (1994). Neurobiology of associative learning in the neonate: Early olfactory learning. Behavioral and Neural Biology, 61, 1–18.CrossRefGoogle ScholarPubMed
Winberg, J., & Porter, R. H. (1998). Olfaction and human neonatal behaviour: Clinical implications. Acta Paediatrica, 87, 6–10.CrossRefGoogle ScholarPubMed
Woo, C. C., & Leon, M. (1987). Sensitive period for neural and behavioral response development to learned odors. Developmental Brain Research, 36, 309–313.CrossRefGoogle Scholar
Wright, L. D., Hébert, K. E., & Perrot-Sinal, T. S. (2008). Periadolescent stress exposure exerts long-term effects on adult stress responding and expression of prefrontal dopamine receptors in male and female rats. Psychoneuroendocrinology, 33, 130–142.CrossRefGoogle ScholarPubMed
Yamazaki, K., Beauchamp, G. K., Kupniewski, D., Bard, J., Thomas, L., & Boyse, E. A. (1988). Familial imprinting determines H-2 selective mating preferences. Science, 240, 1331–1332.CrossRefGoogle ScholarPubMed

Accessibility standard: Unknown

Accessibility compliance for the PDF of this book is currently unknown and may be updated in the future.

Save book to Kindle

To save this book 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 saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved 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.

Available formats
×

Save book to Dropbox

To save content items to your account, please 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 account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please 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 account. Find out more about saving content to Google Drive.

Available formats
×