Skip to main content

Unique characteristics of neonatal classical conditioning: The role of the amygdala and locus coeruleus

Abstract

The central nervous system of altricial infants is specialized for optimizing attachments to their caregiver. During the first postnatal days, infant rats show a sensitive period for learning and particularly susceptible to learning an attraction to their mother’s odor. Classical conditioning appears to underlie this learning that is expressed behaviorally as anincreased ability to acquire odor preferences and a decreased ability to acquire odor aversions. Specifically, in neonatal rats, pairing an odor with moderately painful shock (0.5mA) or milk produces a subsequent relativepreference for that odor. The neural circuitry supporting theincreased ability to acquire odor preferences appears to be the heightened functioning of the noradrenergic pontine nucleus locus coeruleus. Indeed, norepinephrine from the locus coeruleus appears to be both necessary and sufficient for learning during the sensitive period. On the other hand, thedecreased ability to acquire odor aversions seems to be due to the lack of participation of the amygdala in at least some aversive learning situations. The site of plasticity in the pup’s brain appears to be limited to the olfactory bulb. This neonatal sensitive period for learning ends around postnatal day 9–10, at which time pups make the transition from crawling to walking and classical conditioning becomes “adultlike”. The neonatal behavioral and neural induced changes are retained into adulthood where it modifies sexual behavior.

This is a preview of subscription content, access via your institution.

References

  • Ader, R., & Peck, J.H. (1977). Early learning and retention of a conditioned taste aversion.Development Psychobiology, 10, 213–218.

    Google Scholar 

  • Alberts, J.R., & May, B. (1984). Nonnutritive, thermotactile induction of filial huddling in rat pups.Developmental Psychobiology, 17: 161–181.

    PubMed  Google Scholar 

  • Aston-Jones G., Rajkowski, J., & Cohen, J. (1999). Role of locus coeruleus in attention and behavioral flexibility.Biologic Psychiatry, 46, 1309–1320.

    Google Scholar 

  • Aston-Jones, G., Rajkowski, J., Kubiak, P. & Alexinsky, R. (1994). Locus coeruleus neurons in the monkey are selectively activated by attended stimuli in a vigilance task.Journal of Neuroscience, 14, 4467–4480.

    PubMed  Google Scholar 

  • Barr, G.A., & Wang, S. (1992). Peripheral and central administration of cocaine produces conditioned odor preferences in the infant rats.Brain Research, 599: 181–185.

    PubMed  Google Scholar 

  • Barr, G.A., and Rossi, G. (1992). Conditioned place preference from ventral tegmental injections of morphine in neonatal rats.Developmental Brain Research, 66, 133–136.

    PubMed  Google Scholar 

  • Bayer, S.A. (1980). Quantitative 3H-thimidine radiographic analysis of neurogenesis in the rat amygdala.The Journal of Comparative Neurology, 194, 845–875.

    PubMed  Google Scholar 

  • Berdel, B., Morys, J., & Maciejewska, B. (1997). Neuronal changes in the basolateral complex during development of the amygdala of the rat.International Journal of Developmental Neuroscience, 15, 755–765.

    PubMed  Google Scholar 

  • Bezin, L., Marcel, D., Rousset, C., Pujol, J.F., & Weissmann, D. (1994b). Quantitative study of tyrosine hydroxylase protein levels within the somatic area of the rat locus coeruleus during postnatal development.Journal of Neuroscience, 14, 7502–7510.

    PubMed  Google Scholar 

  • Bezin L. Marcel D. Rousset C. Pujol JF, Weissmann D. (1994a). Ontogeny of tyrosine hydroxylase levels in the neuropil close to locus coeruleus.Neuroreport, 5, 1809–12.

    PubMed  Google Scholar 

  • Blozovski, D., & Cudennec, A. (1980). Passive avoidance learning in the young rat.Developmental Psychobiology, 13, 513–518.

    PubMed  Google Scholar 

  • Blozovski, D. & Hennocq, N. (1982). Effects of antimuscarinic cholinergic, drugs injected systemically or into the hippocampal-entorhinal area upon passive avoidance learning in young rats.Psychopharmacology, 76, 351–358.

    PubMed  Google Scholar 

  • Bolles, R.C., & Woods, P.J. (1965). The ontogeny of behavior in the albino rat.Animal Behavior, 12, 427–441.

    Google Scholar 

  • Bowlby J (1965).Attachment. New York: Basic Books.

    Google Scholar 

  • Brake S. (1981). Suckling infant rats learn a preference for a novel olfactory stimulus paired with milk delivery.Science, 211, 506–508.

    PubMed  Google Scholar 

  • Brennen, P.A. & Keverne, E.B. (1997). Neural mechanisms of mammalian olfactory learning.Progress in Neurobiology, 51, 451–457.

    Google Scholar 

  • Brunjes, P.C. & Alberts, J.R. (1979). Olfactory stimulation induces filial preferences for huddling in rat pups.Journal of Comparative and Physiological Psychology, 93, 548–555.

    PubMed  Google Scholar 

  • Cahill, L., Weinberger, N.M., Roozendall, B. & McGaugh, J.L. (1999). Is the amygdala a locus of “conditioned fear”? Some questions and caveats.Neuron, 23, 227–228.

    PubMed  Google Scholar 

  • Camp, L.L., & Rudy, J.W. (1988). Changes in the categorization of appetitive and aversive events during postnatal development of the rat.Developmental Psychobiology, 21, 25–42.

    PubMed  Google Scholar 

  • Campbell, B. A. (1984). Reflections on the ontogeny of learning and memory. In R. Kail and N.E. Spear (Eds.) Comparative perspectives on the development of memory (pp23–35) Hillsdale, NJ: Lawrence Erlbaum Associates.

    Google Scholar 

  • Christie, M.J., & Lelinek, H.F. (1993). Dye-coupling among neurons of the rat locus coeruleus during postnatal development.Neuroscience, 56, 127–129.

    Google Scholar 

  • Collier, A.C., Mast, J., Meyer, D.R., & Jacobs, C.E. (1979). Approach-avoidance conflict in preweanling rats: a development study.Animal Learning & Behavior, 7, 514–520.

    Google Scholar 

  • Cornwell-Jones, C., Sobrian, S.K. (1977). Development of odor-guided behavior in Wistar & Sprague-Dawley rat pups.Physiology and Behavior, 19, 685–688.

    PubMed  Google Scholar 

  • Crain, B., Cotman, C., Taylor, D., & Lynch, G. (1973). A quantitative electron microscopic study of synaptogenesis in the dentate gyrus of the rat.Brain Research, 63, 195–204.

    PubMed  Google Scholar 

  • Dahl, D., & Li, J. (1994). Induction of long-lasting potentiation by sequenced applications of isoproterenol.Neuroreport, 31, 657–660.

    Google Scholar 

  • Dominguez, H.D., Lopez, M.F., & Molina, J.C. (1999). Interactions between perinatal and neonatal associative learning defined by contiguous olfactory and tactile stimulation.Neurobiology of Learning and Memory, 71, 272–288.

    PubMed  Google Scholar 

  • Emerich, D.F., Scalzo, F.M., Enters, E.K., Spear, N., & Spear, L. (1985). Effect of 6-hydroxydopamine-induced catecholamine depletion on shock-precipitated wall climbing of infant rat pups.Developmental Psychobiology, 18, 215–227.

    PubMed  Google Scholar 

  • Fanselow, M.S., & LeDoux, J.E. (1999). Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala.Neuron, 23, 229–232.

    PubMed  Google Scholar 

  • Fanselow, M.S., & Rudy, J.W. (1998). Convergence of experimental & developmental approaches to animal learning and memory processes. In: Carew, T.J., Menzel, R., & Shatz, C.J. (eds.)Mechanistic relationships between development and learning (pp. 15–28). J. Wiley & Sons: New York.

    Google Scholar 

  • Fendt, M., & Fanselow, M.S. (1999). The neuroanatomical and neurochemical basis of conditioned fear.Neuroscience and Biobehavioral Review, 23, 743–760.

    Google Scholar 

  • Ferry, B., Roozendaal, B., & McGaugh, J.L. (1999). Role of norepinephrine in mediating stress hormone regulation of long-term memory storage: a critical involvement of the amygdala.Biological Psychiatry, 46, 1140–1152.

    PubMed  Google Scholar 

  • Fillion, T.J., & Blass, E.M. (1986). Infantile experience with suckling odors determined adult sexual behavior in male rats.Science, 231, 729–731.

    PubMed  Google Scholar 

  • Foote, S.L., Aston-Jones, G., & Bloom, F.E. (1980). Impulse activity of locus coeruleus neurons in awake rats and monkey is a function of sensory stimulation and arousal.Proceedings of the National Academy of Science, 77, 3033–3037.

    Google Scholar 

  • Galef, G.G., & Kaner, H.C. (1980). Establishment & maintenance of preference for natural & artificial olfactory stimuli in juvenile rats.Journal of Comparative & Physiological Psychology, 94, 588–595.

    Google Scholar 

  • Gemberling, G.A., & Domjan, M. (1982). Selective associations in one-day-old rats: taste-toxicosis and textureshock aversion learning. Journal ofComparative Physiological Psychology, 96, 105–13.

    Google Scholar 

  • Goldman, P.S. and Tobach, E. (1967). Behavior modification in infant rats.Animal Behavior, 15:559–562

    Google Scholar 

  • Harley, C.W. (1998). Noradrenergic long-term potentiation in the dentate gyrus.Advances in Pharmacology, 42, 952–956.

    PubMed  Google Scholar 

  • Harley, C.W., & Sara, S.J. (1992). Locus coeruleus burst induced by glutamate trigger delayed perforant path spike amplitude potentiation in the dentate gyrus.Experimental Brain Research, 89, 581–587.

    Google Scholar 

  • Harlow, H.F., & Harlow, M.K. (1965). The affectional systems. In: A Schrier, H.F. Harlow & F. Stollnitz (eds.)Behavior of nonhuman primates. Vol. 2. New York: Academic Press.

    Google Scholar 

  • Haroutunian, V., & Campbell, B.A. (1979). Emergence of interoceptive and exteroceptive control of behavior in rats.Science, 205, 927–929.

    PubMed  Google Scholar 

  • Harris, G.C., & Fitzgerald, R.D. (1991). Locus coeruleus involvement in the learning of classically conditioned bradycardia.Journal of Neuroscience, 11, 2314–2320.

    PubMed  Google Scholar 

  • Helfer, M.E., Kempe, R.S. & Krugman, R.D. (1997).The battered child. University of Chicago Press.

  • Hess, E.H. (1962). Ethology: An approach to the complete analysis of behavior. In:New directions in psychology. (eds. Brown, R., Galanter, E., Hess, E.H. & Mendler, G. Holt), Rinehart & Winston: New York.

    Google Scholar 

  • Hofer, M.A. (1981). The roots of human behavior. W. H. Freeman & Co: New York.

    Google Scholar 

  • Hoffman, H. & Spear, N.E. (1989). Facilitation and impairment of conditioning in the preweanling rat after prior exposure to the conditioned stimulus.Animal Learning and Behavior, 1763–1769.

  • Hudson, R. (1993). Olfactory imprinting.Current Opinions in Neurobiology, 3548–552.

  • Hunt P., & Campbell, B.A. (1999). Developmental dissociation of the components of conditioned fear. In: Bouton ME, Fanselow MS, editors. Learning, Motivation, and Cognition:The functional behaviorism of Robert C Bolles, Washington, DC.

  • Hunt, P.S., Hess MF, Campbell BA (1997).Behavioral Neuroscience, 111, 1257–64.

    Google Scholar 

  • Jiang, M.R., Griff, E.R., Ennis, M., Zimmer, L.A., & Shipley, M.T. (1996). Activation of locus coeruleus enhances the responses of olfactory bulb mitral cells to weak olfactory nerve input.Journal of Neuroscience 16, 6319–6329.

    PubMed  Google Scholar 

  • Johanson, I.B., & Hall, W.G. (1979). Appetitive, learning in I-day-old rat pups.Science, 2054, 19–421.

    Google Scholar 

  • Johanson, I.B., & Teicher, M. (1980). Classical conditioning of an odor preference in 3-day-old rats.Behavioral and Neural Biology, 29, 132–136.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Kehoe, P., & Blass, E. (1986). Central nervous system mediation of positive and negative reinforcement in neonatal albino rats.Developmental Brain Research, 27, 69–75.

    Google Scholar 

  • Lacaille, J.C., & Harley, C.W. (1985). The action of norepinephrine in the dentate gyrus: beta-mediated facilitation of evoked potentials in vitro.Brain Research, 358, 210–220.

    PubMed  Google Scholar 

  • Landers, M., & Sullivan, R.M. (1999). Vibrissae evoked behavior and conditioning before functional ontogeny of the somatosensory vibrissae cortex.Journal of Neuroscience, 19, 5131–5137.

    PubMed  Google Scholar 

  • Langdon, P.E., Harley, C.W., & McLean, J.H. (1997). Increased β adrenoceptor activation overcomes conditioned olfactory learning induced by serotonin depletion.Developmental Brain, Research, 102, 291–293.

    Google Scholar 

  • Lauder, J.M., & Bloom, F.E. (1974). Ontogeny of monoamine neurons in the locus coeruleus, raphe nuclei and substantia nigra of the rat.Journal of Comparative Neurology, 155, 469–482.

    PubMed  Google Scholar 

  • Leon, M. (1975). Dietary control of maternal pheromone in the lactating rat.Physiol Behav, 14:311–319.

    PubMed  Google Scholar 

  • Liang, K.C. (1998). Pretraining infusion of DSP-4 into the amygdala impaired retention in the inhibitory avoidance task: Involvement of norepinephrine but not serotonin in memory facilitation.Chinese Journal of Physiology, 41, 223–33.

    PubMed  Google Scholar 

  • Lincoln, J., Coopersmith, R., Harris, E.W., Cotman, C.W., & Leon, M. (1988). NMDA receptor activation and early olfactory learning.Brain Research, 467, 309–312.

    PubMed  Google Scholar 

  • Marshall, K.C., Christi, M.M., Finlayson, P.G., & Williams, J.T. (1991). Developmental aspects of the locus coeruleus-noradrenaline system.Progress in Brain Research, 88, 173–185.

    PubMed  Google Scholar 

  • Martin, L.T., & Albert, J.R. (1979). Taste aversion to mother’s milk: the age-related role of nursing in acquisition and expression of a learned association.Journal of Comparative and Physiological Psychology, 93:430–445.

    PubMed  Google Scholar 

  • Martin L.T., Alberts J.R. (1982). Associative learning in neonatal rats revealed by cardiac response patterns.Journal of Comparative and physiological psychology, 668–75.

  • McGaugh, J.L., Cahill, L., & Rooszendall, B. (1996). Involvement of the amygdala in memory storage Interaction with other brain systems.Proceedings of the National Academy of Science, 93, 13508–13514.

    Google Scholar 

  • McLean, J.H., & Shipley, M.T. (1991). Postnatal development of the noradrenergic projection from the locus coeruleus to the olfactory bulb in the rat.Journal of Comparative Neurology, 304, 469–477.

    Google Scholar 

  • McLean, J.H., Darby-King, A., Sullivan, R.M., & King, S.R. (1993). Serotonergic influences on olfactory learning in the neonatal rat.Behavioral and Neural Biology, 60, 152–162.

    PubMed  Google Scholar 

  • McLean, J.H., Harley, C.W., Darby-King, A., & Yuan, Q. (1999). pCREB in the neonate rat olfactory bulb is selectively and transiently increased by odor preference-conditioned training.Learning & Memory, 6, 608–618.

    Google Scholar 

  • Mickley, G.A., Schaldach, M.A., Snyder, K.J., Balagh, S.A., Len, T., Neimanis, K., Gaulis, P., Hug, J., Sauchak, K., Remmers-Roeber, D.R., Walker, C., & Yamamoto, B.K. (1998). Ketamine blocks a conditioned taste aversion in neonatal rats.Physiology and Behavior, 64, 381–390.

    PubMed  Google Scholar 

  • Miller, J.S., Jagielo, J.A., & Spear, N.E. (1989). Age-related differences in short-term retention of separable elements of an odor aversion.Journal of Experimental Psychology, 15, 194–201.

    PubMed  Google Scholar 

  • Mizukawa, K., Tseng, I-Ming, & Otsuka, N. (1989). Quantitative electron microscopic analysis of postnatal development of zinc-positive nerve endings in the rat amygdala using Timm’s sulphide silver technique.Developmental Brain Research, 50, 197–203.

    PubMed  Google Scholar 

  • Moffat, S.D., Suh, E.J., & Fleming, A. (1993). Noradrenergic involvement in the consolidation of maternal experience in postpartum rats.Physiology and Behavior, 53, 805–811.

    PubMed  Google Scholar 

  • Moore, C.L., Jordan, L., & Wong, L. (1996). Early olfactory experience, novelty and choice of sexual partner by male rats.Physiology and Behavior, 60, 1361–1367.

    PubMed  Google Scholar 

  • Moriceau, S., Wilson, D.A., & Sullivan, R.M. (2000). Reinstating the neonatal sensitive period for olfactory learning.International Society for Developmental Psychobiology, New Orleans.

  • Myslivecek, J. (1997). Inhibitory learning and memory in newborn rats.Progress in Neurobiology, 53, 399–430.

    PubMed  Google Scholar 

  • Nair, H.P., & Gonzalez-Lima, F. (1999). Extinction of behavior in infant rats: Development of functional coupling between septal, hippocampal, and ventral tegmental regions.Journal of Neuroscience, 19, 8646–8655.

    PubMed  Google Scholar 

  • Nakamura, S., Kimura, F., & Sakaguchi, T. (1987). Postnatal development of electrical activity in the locus coeruleus.Journal of Neurophysiology, 58, 510–24.

    PubMed  Google Scholar 

  • Nakamura, S.T., & Sakaguchi, T. (1990). Development and plasticity of the locus coeruleus. A review of recent physiological and pharmacological experimentation.Progress in Neurobiology, 34, 505–526.

    PubMed  Google Scholar 

  • Okutani, F., Yagi, F., Kaba, H. (1999): Gabaergic control of olfactory learning in young rats.Neuroscience, 93, 1297–300.

    PubMed  Google Scholar 

  • Pager, J. (1974). A selective modulation of olfactory bulb electrical activity in relation to the learning of palatability in hungry and satiated rats.Physiology and Behavior, 12, 189–195.

    PubMed  Google Scholar 

  • Pedersen, P., Williams, C.L., & Blass, E.M. (1982). Activation and odor conditioning of suckling behavior in 3-day-old albino rats.Journal of Experimental Psychology: Animal Behavior Process, 8, 329–341.

    Google Scholar 

  • Rajecki, D.W., Lamb, M.E., & Obmascher, P. (1978).The Behavioral and Brain Sciences, 3, 417–464.

    Google Scholar 

  • Rangel, S., & Leon, M. (1995). Early odor preference training increases olfactory bulb norepinephrine.Developmental Brain Research, 85, 187–191.

    PubMed  Google Scholar 

  • Roth, T., & Sullivan, R. M. (2001). Endogenous opioids and their role in odor preference acquisition and consolidation following odor-shock conditioning in infant rats.Developmental Psychobiology, 39: 188–198.

    PubMed  Google Scholar 

  • Rudy, J.W., & Cheatle, M.D. (1977). Odor aversion learning in neonatal rats.Science, 198, 845–846.

    PubMed  Google Scholar 

  • Rudy, J.W., & Cheatle, M.D. (1978). A role for conditioned stimulus duration in, toxiphobia conditioning.Journal of Experimental Psychology: Animal Behavior Process, 4, 399–411.

    Google Scholar 

  • Rudy, J.W., & Morledge, P. (1994). The ontogeny of contextual fear conditioning: Implications for consolidation, infantile amnesia, and hippocampal system function.Behavioral Neuroscience, 108, 227–234.

    PubMed  Google Scholar 

  • Rudy, J.W., Stadler-Morris, S., & Alberts, P.A. (1987). Ontogeny of spatial navigation behaviors in the rat: Dissociation of “proximal-” and “distal-cue” based behaviors.Behavioral Neuroscience, 101, 62–73.

    PubMed  Google Scholar 

  • Salzen, E.A. (1970). Imprinting and environmental learning. In: Aronson, L.R., Tobach, E., Lehrman, D.S. & Rosensblatt, J. (eds.),Development and Evolution of Behavior. W.H. Feedman: San Francisco.

    Google Scholar 

  • Sananes, C.B., & Campbell, B.A. (1989). Role of the central nucleus of the amygdala in olfactory heart rate conditioning.Behavioral Neuroscience, 103, 519–525.

    PubMed  Google Scholar 

  • Sananes, C.B., Gaddy, J.R., & Campbell, B.A. (1988). Ontogeny of conditioned heart rate to an olfactory stimulus.Developmental Psychobiology 21, 117–33.

    PubMed  Google Scholar 

  • Sara, S.J., Dyon-Laurent, D., & Herve, A. (1995). Novelty seeking behavior in the rat is dependent upon the integrity of the of the noradrenergic system.Cognitive Brain, Research, 2, 181–187.

    Google Scholar 

  • Schoenbaum, G., Chiba, A.A., & Gallagher, M. (1999). Neural encoding in orbitofrontal cortex and basolateral amygdala during olfactory discrimination learning.Journal of Neuroscience, 19, 1876–1884.

    PubMed  Google Scholar 

  • Spear, N.E., Kucharski, D., & Miller, J.S. (1989). The CS-effect in simple conditioning and stimulus selection during development.Animal Learning and Behavior, 17:70–82.

    Google Scholar 

  • Stanton, M.E. (2000). Multiple memory systems, development and conditioning.Behavioral Brain Research, 110, 25–37.

    Google Scholar 

  • Stehouwer, D.J., & Campbell, B.A. (1978). Habituation of the forelimb-withdrawal response in neonatal rats.Journal of Experimental Psychology: Animal Behavior Processes, 4, 104–119.

    PubMed  Google Scholar 

  • Sullivan, R.M., Brake, S.C., Hofer, M.A., & Williams, C.L. (1986a). Huddling and independent feeding of neonatal rats can be facilitated by a conditioned change in behavioral state.Developmental Psychobiology, 19, 625–635.

    PubMed  Google Scholar 

  • Sullivan, R.M., and Hall, W.G. (1988). Reinforcement in infancy: Classical conditioning using tactile stroking or intra-oral milk infusions as UCS.Developmental Psychobiology, 20:215–223.

    Google Scholar 

  • Sullivan, R.M., Hofer, M.A., & Brake, S.C. (1986b). Olfactory-guided orientation in neonatal rats is enhanced by a conditioned change in behavioral state.Developmental Psychobiology, 19:615–623.

    PubMed  Google Scholar 

  • Sullivan, R.M., Landers, M., Yeaman, B., & Wilson, D.A. (2000a). Good memories of bad events in infancy: Ontogeny of conditioned fear and the amygdala.Nature, 407, 38–39.

    PubMed  Google Scholar 

  • Sullivan, R.M., & Leon, M. (1986). Early olfactory learning induces an enhanced olfactory bulb response in young rats.Developmental Brain Research, 27, 278–282.

    Google Scholar 

  • Sullivan, R.M., & Wilson, D.A. (1993). Role of the amygdala complex in, early olfactory associative learning.Behavioral Neuroscience, 107, 254–263.

    PubMed  Google Scholar 

  • Sullivan, R.M., & Wilson, D.A. (1995). Dissociation of behavioral and neural correlates of early associative learning.Developmental Psychobiology, 28, 213–219.

    PubMed  Google Scholar 

  • Sullivan, R.M., Stackenwalt, G., Nasr, F., Lemon, C., & Wilson, D.A. (2000b). Association of an odor with activation of olfactory bulb noradrenergic β-receptors or locus coeruleus stimulation is sufficient to produce learned approach response to that odor in neonatal rats.Behavioral Neuroscience, 114, 957–962.

    PubMed  Google Scholar 

  • Sullivan, R.M., Wilson, D.A., Lemon, C. & Gerhardt, G.A. (1994). Bilateral 6-OHDA lesions of the locus coeruleus impair associative olfactory learning in newborn rats.Brain Research, 643, 306–309.

    PubMed  Google Scholar 

  • Sullivan, R.M., Wilson, D.A., Wong, R., Correa, A., & Leon, M. (1990). Modified behavioral olfactory bulb responses to maternal odors in preweanling rats.Developmental Brain Research, 53, 243–247.

    PubMed  Google Scholar 

  • Sullivan, R.M., Zyzak, D., Skierkowski, P., & Wilson, D.A. (1992). The role of olfactory bulb norepinephrine in early, olfactory learning.Developmental Brain Research, 70, 279–282.

    PubMed  Google Scholar 

  • Takahashi, LK (1994). Stimulus control of behavioral inhibition in the preweanling rat.Physiology and Behavior, 55, 717–21.

    PubMed  Google Scholar 

  • Terry, L.M., & Johanson, I.B. (1996). Effects of altered olfactory experiences on the development of infant rats’ responses to odors.Developmental Psychobiology, 29, 353–377.

    PubMed  Google Scholar 

  • Trombley P.Q., & Shepherd G.M. (1992). Noradrenergic inhibition of synaptic transmission between mitral and granule cells in mammalian olfactory bulb cultures.Journal of Neuroscience, 12, 3985–3991.

    PubMed  Google Scholar 

  • Vankov A, Herve-Minvielle A., & Sara S.J. (1995). Response to novelty and its rapid habituation in locus coeruleus neurons of the freely, exploring rat.European Journal of Neuroscience, 7, 1180–1187.

    PubMed  Google Scholar 

  • Verwer R.W., Van Vulpen E.H., & Van Uum J.F. (1996). Prefrontal development of amygdaloid projections to the prefrontal cortex in the rat studied with retrograde and anterograde tracers.Journal of Comparative Neurology, 376, 75–96.

    PubMed  Google Scholar 

  • Weldon D.A., Travis M.L., & Kennedy D.A. (1991). Postraining DI receptor blockade impairs odor conditioning in neonatal rats.Behavioral Neuroscience, 105, 450–458.

    PubMed  Google Scholar 

  • Wiedenmayer, C.P., & Barr, G.A. (1998). Ontogeny of defensive behavior and analgesia in rat pups exposed to an adult male rat.Physiology and Behavior, 63, 261–9.

    PubMed  Google Scholar 

  • Wilson, D.A., & Leon, M. (1988a). Spatial patterns of olfactory bulb single-unit responses to learned olfactory cues in young rats.Journal of Neurophysiology, 59, 1770–1782.

    PubMed  Google Scholar 

  • Wilson, D.A., & Leon, M. (1988b). Noradrenergic modulation of olfactory bulb excitability in the postnatal rat.Developmental Brain Research, 42, 69–75.

    Google Scholar 

  • Wilson, D.A., & Sullivan, R.M. (1991). Olfactory associative conditioning in infant rats with brain stimulation as reward II: Norepinephrine mediates a specific component of the bulb response to reward.Behavioral Neuroscience, 105, 843–849.

    PubMed  Google Scholar 

  • Wilson, D.A., & Sullivan, R.M. (1992). Blockade of mitral/tufted cell habituation to odors by association with reward: A preliminary note.Brain Research, 594, 143–145.

    PubMed  Google Scholar 

  • Wilson, D.A., Sullivan, R.M., & Leon M. (1987). Single-unit analysis of postnatal olfactory learning: Modified olfactory bulb output response patterns to learned attractive odors.Journal of Neuroscience, 7, 3154–3162.

    PubMed  Google Scholar 

  • Wilson, D.A., & Sullivan, R.M. (1990). Olfactory associative conditioning in infant rats with brain stimulation as reward. I. Neurobehavioral consequences.Developmental Brain Research, 53, 215–221.

    PubMed  Google Scholar 

  • Woo, C.C., & Leon, M. (1988). Sensitive period for neural and behavioral responses to learned odors.Developmental Brain Research. 36, 309–313.

    Google Scholar 

  • Woo, C.C., Coopersmith, R., & Leon, M. (1987). Localized changes in olfactory bulb morphology associated with early olfactory learning.Journal of Comparative Neurology, 263, 113–125.

    PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Regina M. Sullivan.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sullivan, R.M. Unique characteristics of neonatal classical conditioning: The role of the amygdala and locus coeruleus. Integrative Physiological & Behavioral Science 36, 293–307 (2001). https://doi.org/10.1007/BF02688797

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02688797

Key Words

  • classical conditioning
  • olfactory learning
  • imprinting
  • sensitive period
  • neonatal learning
  • odor conditioning
  • attachment
  • abuse
  • amygdala
  • fear conditioning
  • locus coeruleus
  • norepinephrine