Transitions in infant learning are modulated by dopamine within the amygdala

Behavioral transitions characterize development. Young infant rats paradoxically prefer odors that are paired with shock, but older pups learn aversions. This transition is amygdala and corticosterone dependent. Using microarrays and microdialysis, we found downregulated dopaminergic presynaptic function in the amygdala with preference learning. Corticosterone-injected 8-d-old pups and untreated 12-d-old pups learned aversions and had dopaminergic upregulation in the amygdala. Dopamine injection into the amygdala changed preferences to aversions, whereas dopamine antagonism reinstated preference learning.

[1]  O. Elliot,et al.  Differential Human Handling as Reinforcing Events and as Treatments Influencing Later Social Behavior in Basenji Puppies , 1962 .

[2]  B. Storey THE BATTERED CHILD , 1964, The Medical journal of Australia.

[3]  R. Rescorla Pavlovian conditioning and its proper control procedures. , 1967, Psychological review.

[4]  B. Campbell,et al.  Ontogeny of memory. , 1972, Psychological review.

[5]  B. Campbell,et al.  Habituation of the forelimb-withdrawal response in neonatal rats. , 1978, Journal of experimental psychology. Animal behavior processes.

[6]  B. Campbell,et al.  Emergence of interoceptive and exteroceptive control of behavior in rats. , 1979, Science.

[7]  Alleviation of avoidance deficits by approach alternatives in 10-day old rats , 1979, Physiology & Behavior.

[8]  W. G. Hall,et al.  Feeding and behavioral activation in infant rats. , 1979, Science.

[9]  A. Cudennec,et al.  Passive avoidence learning in the young rat. , 1980, Developmental psychobiology.

[10]  R. Bolles,et al.  The ontogenesis of defensive reactions to shock in preweanling rats. , 1980, Developmental psychobiology.

[11]  E. Blass,et al.  Prenatal and postnatal determinants of the 1st suckling episode in albino rats. , 1982, Developmental psychobiology.

[12]  N. Spear,et al.  Effects of 6-hydroxydopamine-induced catecholamine depletion on shock-precipitated wall climbing of infant rat pups. , 1985, Developmental psychobiology.

[13]  B. McEwen,et al.  The development of the glucocorticoid receptor system in the rat limbic brain. I. Ontogeny and autoregulation. , 1985, Brain research.

[14]  K. Fuxe,et al.  Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[15]  E. Blass,et al.  Infantile experience with suckling odors determines adult sexual behavior in male rats. , 1986, Science.

[16]  M. Leon,et al.  Enhanced neural response by adult rats to odors experienced early in life , 1986, Brain Research.

[17]  R. Sullivan,et al.  Early olfactory learning induces an enhanced olfactory bulb response in young rats. , 1986, Brain research.

[18]  R. Rescorla Behavioral studies of Pavlovian conditioning. , 1988, Annual review of neuroscience.

[19]  B. Campbell,et al.  Role of the central nucleus of the amygdala in olfactory heart rate conditioning. , 1989, Behavioral neuroscience.

[20]  N. Spear,et al.  Ontogenetic differences in the association of gustatory and tactile cues with lithium chloride and footshock. , 1990, Behavioral and neural biology.

[21]  G. Barr,et al.  Developmental psychobiology : new methods and changing concepts , 1991 .

[22]  D. Wilson,et al.  Neural correlates of conditioned odor avoidance in infant rats. , 1991, Behavioral neuroscience.

[23]  George Paxinos,et al.  Atlas Of The Developing Rat Brain , 1991 .

[24]  Joseph E LeDoux,et al.  Corticosterone Potentiation of Conditioned Fear in Rats a , 1994, Annals of the New York Academy of Sciences.

[25]  G. Barr Ontogeny of nociception and antinociception. , 1995, NIDA research monograph.

[26]  P. Overton,et al.  Preferential occupation of mineralocorticoid receptors by corticosterone enhances glutamate-induced burst firing in rat midbrain dopaminergic neurons , 1996, Brain Research.

[27]  J. D. McGaugh,et al.  Adrenocortical suppression blocks the memory-enhancing effects of amphetamine and epinephrine. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[28]  C. L. Moore,et al.  Early Olfactory Experience, Novelty, and Choice of Sexual Partner by Male Rats , 1996, Physiology & Behavior.

[29]  Younglim Lee,et al.  Roles of the Amygdala and Bed Nucleus of the Stria Terminalis in Fear and Anxiety Measured with the Acoustic Startle Reflex , 1997, Annals of the New York Academy of Sciences.

[30]  M. Fleshner,et al.  A selective role for corticosterone in contextual-fear conditioning. , 1997, Behavioral Neuroscience.

[31]  T. Otto,et al.  Odor-guided fear conditioning in rats: 2. Lesions of the anterior perirhinal cortex disrupt fear conditioned to the explicit conditioned stimulus but not to the training context. , 1997, Behavioral neuroscience.

[32]  M. Hofer,et al.  Potentiation and inhibition of ultrasonic vocalization of rat pups: regulation by social cues. , 1997, Developmental psychobiology.

[33]  Joseph E LeDoux,et al.  Why We Think Plasticity Underlying Pavlovian Fear Conditioning Occurs in the Basolateral Amygdala , 1999, Neuron.

[34]  D. Maestripieri,et al.  Consistency and change in the behavior of rhesus macaque abusive mothers with successive infants. , 1999, Developmental psychobiology.

[35]  M. Stanton Multiple memory systems, development and conditioning , 2000, Behavioural Brain Research.

[36]  R. Sullivan,et al.  Neurophysiology: Good memories of bad events in infancy , 2000, Nature.

[37]  M. Stanton,et al.  Ontogenetic differences in the effects of unpaired stimulus preexposure on eyeblink conditioning in the rat. , 2001, Developmental psychobiology.

[38]  P. Plotsky,et al.  Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models , 2001, Development and Psychopathology.

[39]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[40]  T. Otto,et al.  Patterns of Fos expression in the amygdala and ventral perirhinal cortex induced by training in an olfactory fear conditioning paradigm. , 2001, Behavioral neuroscience.

[41]  H. T. Blair,et al.  Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. , 2001, Learning & memory.

[42]  A. Grace,et al.  Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning , 2002, Nature.

[43]  Benno Roozendaal,et al.  Stress and Memory: Opposing Effects of Glucocorticoids on Memory Consolidation and Memory Retrieval , 2002, Neurobiology of Learning and Memory.

[44]  R D Spealman,et al.  Cocaine Administered into the Medial Prefrontal Cortex Reinstates Cocaine-Seeking Behavior by Increasing AMPA Receptor-Mediated Glutamate Transmission in the Nucleus Accumbens , 2002, The Journal of Neuroscience.

[45]  Michael Davis,et al.  Role of the Amygdala in Fear Extinction Measured with Potentiated Startle , 2003, Annals of the New York Academy of Sciences.

[46]  Hans-Christian Pape,et al.  Genes and Mechanisms in the Amygdala Involved in the Formation of Fear Memory , 2003, Annals of the New York Academy of Sciences.

[47]  Stephen Maren The Amygdala, Synaptic Plasticity, and Fear Memory , 2003, Annals of the New York Academy of Sciences.

[48]  Greg D. Gale,et al.  The Amygdala, Fear, and Memory , 2003, Annals of the New York Academy of Sciences.

[49]  Y. Humeau,et al.  Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition , 2003, Nature Neuroscience.

[50]  Dagmar Galter,et al.  ALDH1 mRNA: presence in human dopamine neurons and decreases in substantia nigra in Parkinson's disease and in the ventral tegmental area in schizophrenia , 2003, Neurobiology of Disease.

[51]  Rainer Breitling,et al.  Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments , 2004, FEBS letters.

[52]  B. Everitt,et al.  Direct Interactions between the Basolateral Amygdala and Nucleus Accumbens Core Underlie Cocaine-Seeking Behavior by Rats , 2004, The Journal of Neuroscience.

[53]  J. Schulkin,et al.  Corticosterone facilitates retention of contextually conditioned fear and increases CRH mRNA expression in the amygdala , 2004, Behavioural Brain Research.

[54]  Benno Roozendaal,et al.  Memory enhancement of classical fear conditioning by post-training injections of corticosterone in rats , 2004, Neurobiology of Learning and Memory.

[55]  R. Gervais,et al.  Olfactory fear conditioning induces field potential potentiation in rat olfactory cortex and amygdala. , 2004, Learning & memory.

[56]  Maria Fitzgerald,et al.  The development of nociceptive circuits , 2005, Nature Reviews Neuroscience.

[57]  James L McGaugh,et al.  Memory enhancement induced by post-training intrabasolateral amygdala infusions of beta-adrenergic or muscarinic agonists requires activation of dopamine receptors: Involvement of right, but not left, basolateral amygdala. , 2005, Learning & memory.

[58]  S. Lindell,et al.  Neurobiological characteristics of rhesus macaque abusive mothers and their relation to social and maternal behavior , 2005, Neuroscience & Biobehavioral Reviews.

[59]  R. Sullivan,et al.  Memory of early maltreatment: Neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning , 2005, Biological Psychiatry.

[60]  S. Moriceau,et al.  Maternal presence serves as a switch between learning fear and attraction in infancy , 2006, Nature Neuroscience.

[61]  S. Moriceau,et al.  Dual Circuitry for Odor–Shock Conditioning during Infancy: Corticosterone Switches between Fear and Attraction via Amygdala , 2006, The Journal of Neuroscience.

[62]  Joseph E. LeDoux,et al.  Long-term potentiation in the amygdala: A cellular mechanism of fear learning and memory , 2007, Neuropharmacology.

[63]  Parker J. Holman,et al.  Enduring Effects of Infant Memories: Infant Odor-Shock Conditioning Attenuates Amygdala Activity and Adult Fear Conditioning , 2007, Biological Psychiatry.

[64]  S. Moriceau,et al.  Maternal attenuation of hypothalamic paraventricular nucleus norepinephrine switches avoidance learning to preference learning in preweanling rat pups , 2007, Hormones and Behavior.

[65]  E. Kandel,et al.  An Animal Model of a Behavioral Intervention for Depression , 2008, Neuron.

[66]  R. Sullivan,et al.  Neonatal odor-shock conditioning alters the neural network involved in odor fear learning at adulthood. , 2008, Learning & memory.

[67]  G. Fink ENCYCLOPEDIA OF STRESS , 2000, Experimental Neurology.

[68]  A. Lüthi,et al.  Switching on and off fear by distinct neuronal circuits , 2008, Nature.

[69]  R. Sullivan,et al.  Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity , 2008, Brain Research.

[70]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[71]  S. Moriceau,et al.  Developing a Neurobehavioral Animal Model of Infant Attachment to an Abusive Caregiver , 2010, Biological Psychiatry.