Advertisement
Priority Communication| Volume 78, ISSUE 3, P159-166, August 01, 2015

Differences in Stress-Induced Changes in Extinction and Prefrontal Plasticity in Postweanling and Adult Animals

  • Rachel Schayek
    Affiliations
    Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa Israel.
    Search for articles by this author
  • Mouna Maroun
    Correspondence
    Address correspondence to Mouna Maroun, Ph.D., University of Haifa, Sagol Department of Neurobiology, Faculty of Natural Sciences, Haifa 3498838, Israel
    Affiliations
    Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa Israel.
    Search for articles by this author

      Abstract

      Background

      Postweaning is a critical developmental stage during which the medial prefrontal cortex (mPFC) undergoes major changes and the brain is vulnerable to the effects of stress. Surprisingly, the engagement of the mPFC in extinction of fear was reported to be identical in postweanling (PW) and adult animals. Here, we examined whether the effect of stress on extinction and mPFC plasticity would be similar in PW and adult animals.

      Methods

      PW and adult animals were fear conditioned and exposed to the elevated platform stress paradigm, and extinction and long-term potentiation were examined. The dependency of stress-induced modulation of extinction and plasticity on N-methyl-D-aspartate receptors was examined as well.

      Results

      We show that exposure to stress is associated with reduction of fear and enhanced induction of long-term potentiation (LTP) in PW pups, in contrast to its effects in adult animals. Furthermore, we report opposite effects in the occlusion of LTP following the enhanced or impaired extinction in the two age groups and that the reversal of the effects of stress is independent of N-methyl-D-aspartate receptor activation in PW animals.

      Conclusions

      Our results show that qualitatively different mechanisms control the modulatory effects of stress on extinction and plasticity in postweanling pups compared with adult rats. Our results point to significant differences between young and adult brains, which may have potential implications for the treatment of anxiety and stress disorders across development.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Biological Psychiatry
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Milad M.R.
        • Quirk G.J.
        Neurons in medial prefrontal cortex signal memory for fear extinction.
        Nature. 2002; 420: 70-74
        • Santini E.
        • Ge H.
        • Ren K.
        • Pena de Ortiz S.
        • Quirk G.J.
        Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex.
        J Neurosci. 2004; 24: 5704-5710
        • Hugues S.
        • Chessel A.
        • Lena I.
        • Marsault R.
        • Garcia R.
        Prefrontal infusion of PD098059 immediately after fear extinction training blocks extinction-associated prefrontal synaptic plasticity and decreases prefrontal ERK2 phosphorylation.
        Synapse. 2006; 60: 280-287
        • Akirav I.
        • Maroun M.
        The role of the medial prefrontal cortex-amygdala circuit in stress effects on the extinction of fear.
        Neural Plast. 2007; 2007: 30873
        • Herry C.
        • Ciocchi S.
        • Senn V.
        • Demmou L.
        • Muller C.
        • Luthi A.
        Switching on and off fear by distinct neuronal circuits.
        Nature. 2008; 454: 600-606
        • Moriceau S.
        • Wilson D.A.
        • Levine S.
        • Sullivan R.M.
        Dual circuitry for odor-shock conditioning during infancy: Corticosterone switches between fear and attraction via amygdala.
        J Neurosci. 2006; 26: 6737-6748
      1. Dumas TC, Rudy JW (2010): Development of the hippocampal memory system: Creating networks and modifiable synapses. In: Blumberg MS, Freeman JH, Jr, Robinson SR, editors. Oxford handbook of developmental behavioral neuroscience. New York: Oxford University Press, 587–606.

        • Burman M.
        • Murawski N.
        • Schiffino F.
        • Rosen J.
        • Stanton M.
        Factors governing single-trial contextual fear conditioning in the weanling rat.
        Behav Neurosci. 2009; 123: 1148-1152
        • Rudy J.W.
        Contextual conditioning and auditory cue conditioning dissociate during development.
        Behav Neurosci. 1993; 107: 887-891
        • Rudy J.W.
        • Morledge P.
        Ontogeny of contextual fear conditioning in rats: Implications for consolidation, infantile amnesia, and hippocampal system function.
        Behav Neurosci. 1994; 108: 227-234
        • Stanton M.E.
        Multiple memory systems, development and conditioning.
        Behav Brain Res. 2000; 110: 25-37
        • Schiffino F.L.
        • Murawski N.J.
        • Rosen J.B.
        • Stanton M.E.
        Ontogeny and neural substrates of the context preexposure facilitation effect.
        Neurobiol Learn Mem. 2011; 95: 190-198
        • Jernigan T.L.
        • Trauner D.A.
        • Hesselink J.R.
        • Tallal P.A.
        Maturation of human cerebrum observed in vivo during adolescence.
        Brain. 1991; 114: 2037-2049
        • Giedd J.N.
        • Vaituzis A.C.
        • Hamburger S.D.
        • Lange N.
        • Rajapakse J.C.
        • Kaysen D.
        • et al.
        Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4–18 years.
        J Comp Neurol. 1996; 366: 223-230
        • Giedd J.N.
        • Snell J.W.
        • Lange N.
        • Rajapakse J.C.
        • Casey B.J.
        • Kozuch P.L.
        • et al.
        Quantitative magnetic resonance imaging of human brain development: Ages 4-18.
        Cereb Cortex. 1996; 6: 551-560
        • Sowell E.R.
        • Thompson P.M.
        • Holmes C.J.
        • Jernigan T.L.
        • Toga A.W.
        In vivo evidence for post-adolescent brain maturation in frontal and striatal regions.
        Nat Neurosci. 1999; 2: 859-861
        • Markham J.A.
        • Morris J.R.
        • Juraska J.M.
        Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood.
        Neuroscience. 2007; 144: 961-968
        • Rubinow M.J.
        • Juraska J.M.
        Neuron and glia numbers in the basolateral nucleus of the amygdala from preweaning through old age in male and female rats: A stereological study.
        J Comp Neurol. 2009; 512: 717-725
        • Gao W.J.
        • Wormington A.B.
        • Newman D.E.
        • Pallas S.L.
        Development of inhibitory circuitry in visual and auditory cortex of postnatal ferrets: Immunocytochemical localization of calbindin‐and parvalbumin‐containing neurons.
        J Comp Neurol. 2000; 422: 140-157
        • Tseng K.Y.
        • O׳Donnell P.
        Dopamine modulation of prefrontal cortical interneurons changes during adolescence.
        Cereb Cortex. 2007; 17: 1235-1240
        • Kumar S.S.
        • Huguenard J.R.
        Pathway-specific differences in subunit composition of synaptic NMDA receptors on pyramidal neurons in neocortex.
        J Neurosci. 2003; 23: 10074-10083
        • Liu X.B.
        • Murray K.D.
        • Jones E.G.
        Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development.
        J Neurosci. 2004; 24: 8885-8895
        • Spear L.P.
        The adolescent brain and age-related behavioral manifestations.
        Neurosci Biobehav Rev. 2000; 24: 417-463
        • van Eden C.G.
        • Kros J.M.
        • Uylings H.B.
        The development of the rat prefrontal cortex. Its size and development of connections with thalamus, spinal cord and other cortical areas.
        Prog Brain Res. 1990; 85: 169-183
        • Benes F.M.
        • Todtenkopf M.S.
        • Logiotatos P.
        • Williams M.
        Glutamate decarboxylase(65)-immunoreactive terminals in cingulate and prefrontal cortices of schizophrenic and bipolar brain.
        J Chem Neuroanat. 2000; 20: 259-269
        • Wiedenmayer C.P.
        • Magariños A.M.
        • McEwen B.S.
        • Barr G.A.
        Age-specific threats induce CRF expression in the paraventricular nucleus of the hypothalamus and hippocampus of young rats.
        Horm Behav. 2005; 47: 139-150
        • Chan T.
        • Kyere K.
        • Davis B.R.
        • Shemyakin A.
        • Kabitzke P.A.
        • Shair H.N.
        • et al.
        The role of the medial prefrontal cortex in innate fear regulation in infants, juveniles, and adolescents.
        J Neurosci. 2011; 31: 4991-4999
        • Vazquez D.M.
        Stress and the developing limbic-hypothalamic-pituitary-adrenal axis.
        Psychoneuroendocrinology. 1998; 23: 663-700
        • Romeo R.D.
        • Lee S.J.
        • Chhua N.
        • McPherson C.R.
        • McEwen B.S.
        Testosterone cannot activate an adult-like stress response in prepubertal male rats.
        Neuroendocrinology. 2004; 79: 125-132
        • Giedd J.N.
        Structural magnetic resonance imaging of the adolescent brain.
        Ann N Y Acad Sci. 2004; 1021: 77-85
        • Gogtay N.
        • Giedd J.N.
        • Lusk L.
        • Hayashi K.M.
        • Greenstein D.
        • Vaituzis A.C.
        • et al.
        Dynamic mapping of human cortical development during childhood through early adulthood.
        Proc Natl Acad Sci U S A. 2004; 101: 8174-8179
        • Suzuki M.
        • Zhou S.Y.
        • Takahashi T.
        • Hagino H.
        • Kawasaki Y.
        • Niu L.
        • et al.
        Differential contributions of prefrontal and temporolimbic pathology to mechanisms of psychosis.
        Brain. 2005; 128: 2109-2122
        • Maroun M.
        • Richter-Levin G.
        Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo.
        J Neurosci. 2003; 23: 4406-4409
        • Richter-Levin G.
        • Maroun M.
        Stress and amygdala suppression of metaplasticity in the medial prefrontal cortex.
        Cereb Cortex. 2010; 20: 2433-2441
        • Rocher C.
        • Spedding M.
        • Munoz C.
        • Jay T.M.
        Acute stress-induced changes in hippocampal/prefrontal circuits in rats: Effects of antidepressants.
        Cereb Cortex. 2004; 14: 224-229
        • Izquierdo A.
        • Wellman C.L.
        • Holmes A.
        Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice.
        J Neurosci. 2006; 26: 5733-5738
        • Akirav I.
        • Segev A.
        • Motanis H.
        • Maroun M.
        D-cycloserine into the BLA reverses the impairing effects of exposure to stress on the extinction of contextual fear, but not conditioned taste aversion.
        Learn Mem. 2009; 16: 682-686
        • Maroun M.
        • Ioannides P.J.
        • Bergman K.L.
        • Kavushansky A.
        • Holmes A.
        • Wellman C.L.
        Fear extinction deficits following acute stress associate with increased spine density and dendritic retraction in basolateral amygdala neurons.
        Eur J Neurosci. 2013; 38: 2611-2620
        • Rioult-Pedotti M.S.
        • Friedman D.
        • Donoghue J.P.
        Learning-induced LTP in neocortex.
        Science. 2000; 290: 533-536
        • Monfils M.
        • Teskey G.
        Skilled-learning-induced potentiation in rat sensorimotor cortex: A transient form of behavioural long-term potentiation.
        Neuroscience. 2004; 125: 329-336
        • Whitlock J.R.
        • Heynen A.J.
        • Shuler M.G.
        • Bear M.F.
        Learning induces long-term potentiation in the hippocampus.
        Science. 2006; 313: 1093-1097
        • Schmidt M.
        • Abraham W.
        • Maroun M.
        • Stork O.
        • Richter-Levin G.
        Stress-induced metaplasticity: From synapses to behavior.
        Neuroscience. 2013; 250: 112-120
        • Langton J.M.
        • Kim J.H.
        • Nicholas J.
        • Richardson R.
        The effect of the NMDA receptor antagonist MK-801 on the acquisition and extinction of learned fear in the developing rat.
        Learn Mem. 2007; 14: 665-668
        • Gogolla N.
        • Caroni P.
        • Luthi A.
        • Herry C.
        Perineuronal nets protect fear memories from erasure.
        Science. 2009; 325: 1258-1261
        • Kim J.H.
        • Hamlin A.S.
        • Richardson R.
        Fear extinction across development: The involvement of the medial prefrontal cortex as assessed by temporary inactivation and immunohistochemistry.
        J Neurosci. 2009; 29: 10802-10808
        • Miracle A.D.
        • Brace M.F.
        • Huyck K.D.
        • Singler S.A.
        • Wellman C.L.
        Chronic stress impairs recall of extinction of conditioned fear.
        Neurobiol Learn Mem. 2006; 85: 213-218
        • Garcia R.
        • Spennato G.
        • Nilsson-Todd L.
        • Moreau J.
        • Deschaux O.
        Hippocampal low-frequency stimulation and chronic mild stress similarly disrupt fear extinction memory in rats.
        Neurobiol Learn Mem. 2008; 89: 560-566
        • Farrell M.R.
        • Sayed J.A.
        • Underwood A.R.
        • Wellman C.L.
        Lesion of infralimbic cortex occludes stress effects on retrieval of extinction but not fear conditioning.
        Neurobiol Learn Mem. 2010; 94: 240-246
        • Wilber A.A.
        • Walker A.G.
        • Southwood C.J.
        • Farrell M.R.
        • Lin G.L.
        • Rebec G.V.
        • Wellman C.L.
        Chronic stress alters neural activity in medial prefrontal cortex during retrieval of extinction.
        Neuroscience. 2011; 174: 115-131
        • Baran S.E.
        • Armstrong C.E.
        • Niren D.C.
        • Hanna J.J.
        • Conrad C.D.
        Chronic stress and sex differences on the recall of fear conditioning and extinction.
        Neurobiol Learn Mem. 2009; 91: 323-332
        • Jacobson-Pick S.
        • Richter-Levin G.
        Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats.
        Behav Brain Res. 2010; 214: 268-276
        • Dubreucq S.
        • Kambire S.
        • Conforzi M.
        • Metna-Laurent M.
        • Cannich A.
        • Soria-Gomez E.
        • et al.
        Cannabinoid type 1 receptors located on single-minded 1–expressing neurons control emotional behaviors.
        Neuroscience. 2012; 204: 230-244
        • Yuen E.Y.
        • Liu W.
        • Karatsoreos I.N.
        • Feng J.
        • McEwen B.S.
        • Yan Z.
        Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory.
        Proc Natl Acad Sci U S A. 2009; 106: 14075-14079
        • Yuen E.Y.
        • Liu W.
        • Karatsoreos I.N.
        • Ren Y.
        • Feng J.
        • McEwen B.S.
        • Yan Z.
        Mechanisms for acute stress-induced enhancement of glutamatergic transmission and working memory.
        Mol Psychiatry. 2011; 16: 156-170
        • Liu P.
        • Yuen Y.
        • Hsiao H.M.
        • Jaykus L.A.
        • Moe C.
        Effectiveness of liquid soap and hand sanitizer against Norwalk virus on contaminated hands.
        Appl Environ Microbiol. 2010; 76: 394-399
        • Rogan M.T.
        • Stäubli U.V.
        • LeDoux J.E.
        Fear conditioning induces associative long-term potentiation in the amygdala.
        Nature. 1997; 390: 604-607
        • Vouimba R.M.
        • Maroun M.
        Learning-induced changes in mPFC-BLA connections after fear conditioning, extinction, and reinstatement of fear.
        Neuropsychopharmacology. 2011; 36: 2276-2285
        • Jay T.M.
        • Burette F.
        • Laroche S.
        NMDA receptor-dependent long-term potentiation in the hippocampal afferent fibre system to the prefrontal cortex in the rat.
        Eur J Neurosci. 1995; 7: 247-250
        • Moghaddam B.
        Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: Comparison to hippocampus and basal ganglia.
        J Neurochem. 1993; 60: 1650-1657
        • Martin K.P.
        • Wellman C.L.
        NMDA receptor blockade alters stress-induced dendritic remodeling in medial prefrontal cortex.
        Cereb Cortex. 2011; 21: 2366-2373
        • Mockett B.
        • Coussens C.
        • Abraham W.C.
        NMDA receptor-mediated metaplasticity during the induction of long-term depression by low-frequency stimulation.
        Eur J Neurosci. 2002; 15: 1819-1826
        • MacDonald J.F.
        • Jackson M.F.
        • Beazely M.A.
        G protein-coupled receptors control NMDARs and metaplasticity in the hippocampus.
        Biochim Biophys Acta. 2007; 1768: 941-951
        • Rosenblum K.
        • Maroun M.
        • Richter-Levin G.
        Frequency-dependent inhibition in the dentate gyrus is attenuated by the NMDA receptor blocker MK-801 at doses that do not yet affect long-term potentiation.
        Hippocampus. 1999; 9: 491-494
        • Van Eden C.
        • Uylings H.
        Cytoarchitectonic development of the prefrontal cortex in the rat.
        J Comp Neurol. 1985; 241: 253-267
        • Zhang Z.W.
        Maturation of layer V pyramidal neurons in the rat prefrontal cortex: Intrinsic properties and synaptic function.
        J Neurophysiol. 2004; 91: 1171-1182
        • Peter R.
        Synaptic density in human frontal cortex—developmental changes and effects of aging.
        Brain Res. 1979; 163: 195-205
        • Kalsbeek A.
        • Voorn P.
        • Buijs R.
        • Pool C.
        • Uylings H.
        Development of the dopaminergic innervation in the prefrontal cortex of the rat.
        J Comp Neurol. 1988; 269: 58-72
        • Nair H.P.
        • Berndt J.D.
        • Barrett D.
        • Gonzalez-Lima F.
        Maturation of extinction behavior in infant rats: Large-scale regional interactions with medial prefrontal cortex, orbitofrontal cortex, and anterior cingulate cortex.
        J Neurosci. 2001; 21: 4400-4407
        • Li S.
        • Kim J.H.
        • Richardson R.
        Differential involvement of the medial prefrontal cortex in the expression of learned fear across development.
        Behav Neurosci. 2012; 126: 217-225
        • Kim J.H.
        • Richardson R.
        The effect of temporary amygdala inactivation on extinction and reextinction of fear in the developing rat: Unlearning as a potential mechanism for extinction early in development.
        J Neurosci. 2008; 28: 1282-1290
        • Zitman F.
        • Richter-Levin G.
        Age and sex-dependent differences in activity, plasticity and response to stress in the dentate gyrus.
        Neuroscience. 2013; 249: 21-30
        • Spear L.P.
        • Brake S.C.
        Periadolescence: Age-dependent behavior and psychopharmacological responsivity in rats.
        Dev Psychobiol. 1983; 16: 83-109
        • Adriani W.
        • Granstrem O.
        • Macri S.
        • Izykenova G.
        • Dambinova S.
        • Laviola G.
        Behavioral and neurochemical vulnerability during adolescence in mice: studies with nicotine.
        Neuropsychopharmacology. 2004; 29: 869-878
        • Brenhouse H.C.
        • Sonntag K.C.
        • Andersen S.L.
        Transient D1 dopamine receptor expression on prefrontal cortex projection neurons: Relationship to enhanced motivational salience of drug cues in adolescence.
        J Neurosci. 2008; 28: 2375-2382
        • Paus T.
        Growth of white matter in the adolescent brain: Myelin or axon?.
        Brain Cogn. 2010; 72: 26-35