Morphology and dendritic maturation of developing principal neurons in the rat basolateral amygdala

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• 作者：Steven J. Ryan ; David E. Ehrlich ; Donald G. Rainnie
• 关键词：Basal amygdala ; Pyramidal ; Dendritic spine ; Sholl analysis
• 刊名：Brain Structure and Function
• 出版年：2016
• 出版时间：March 2016
• 年：2016
• 卷：221
• 期：2
• 页码：839-854
• 全文大小：2,716 KB
• 参考文献：Adolphs R, Baron-Cohen S, Tranel D (2002) Impaired recognition of social emotions following amygdala damage. J Cogn Neurosci 14(8):1264–1274CrossRef PubMed
  Baas PW, Lin S (2011) Hooks and comets: the story of microtubule polarity orientation in the neuron. Dev Neurobiol 71(6):403–418CrossRef PubMed PubMedCentral
  Ballesteros-Yáñez I, Benavides-Piccione R, Elston GN, Yuste R, DeFelipe J (2006) Density and morphology of dendritic spines in mouse neocortex. Neuroscience 138(2):403–409CrossRef PubMed
  Barnet RC, Hunt PS (2005) Trace and long-delay fear conditioning in the developing rat. Learn Behav 33:437–443CrossRef PubMed
  Barnet RC, Hunt PS (2006) The expression of fear-potentiated startle during development: integration of learning and response systems. Behav Neurosci 120:861–872CrossRef PubMed
  Beckel-Mitchener A, Greenough WT (2004) Correlates across the structural, functional, and molecular phenotypes of fragile X syndrome. Ment Retard Dev D R 10(1):53–59CrossRef
  Berdel B, Moryś J (2000) Expression of calbindin-D28 k and parvalbumin during development of rat’s basolateral amygdaloid complex. Int J Dev Neurosci 18(6):501–513CrossRef PubMed
  Bony G, Szczurkowska J, Tamagno I, Shelly M, Contestabile A, Cancedda L (2013) Non-hyperpolarizing GABAB receptor activation regulates neuronal migration and neurite growth and specification by cAMP/LKB1. Nat Commun 4:1800CrossRef PubMed
  Bouwmeester H, Smits K, Van Ree JM (2002) Neonatal development of projections to the basolateral amygdala from prefrontal and thalamic structures in rat. J Comp Neurol 450(3):241–255CrossRef PubMed
  Brummelte S, Teuchert-Noodt G (2006) Postnatal development of dopamine innervation in the amygdala and the entorhinal cortex of the gerbil (Meriones unguiculatus). Brain Res 1125(1):9–16CrossRef PubMed
  Calabrese B, Wilson MS, Halpain S (2006) Development and regulation of dendritic spine synapses. Physiol (Bethesda) 21:38–47CrossRef
  Camp LL, Rudy JW (1988) Changes in the categorization of appetitive and aversive events during postnatal development of the rat. Dev Psychobiol 21:25–42CrossRef PubMed
  Campbell BA, Ampuero MX (1985) Dissociation of autonomic and behavioral components of conditioned fear during development in the rat. Behav Neurosci 99:1089–1102CrossRef PubMed
  Cancedda L, Fiumelli H, Chen K, Poo M (2007) Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci 27(19):5224CrossRef PubMed
  Chareyron LJ, Banta Lavenex P, Amaral DG, Lavenex P (2011) Stereological analysis of the rat and monkey amygdala. J Comp Neurol 519(16):3218–3239CrossRef PubMed PubMedCentral
  Chareyron LJ, Banta Lavenex P, Lavenex P (2012) Postnatal development of the amygdala: a stereological study in rats. J Comp Neurol 520(16):3745–3763CrossRef PubMed
  Cressman VL, Balaban J, Steinfeld S, Shemyakin A, Graham P, Parisot N, Moore H (2010) Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat. J Comp Neurol 518(14):2693–2709PubMed PubMedCentral
  Davis M, Walker DL, Myers KM (2003) Role of the amygdala in fear extinction measured with potentiated startle. Ann NY Acad Sci 985:218–232CrossRef PubMed
  Ehrlich DE, Ryan SJ, Rainnie DG (2012) Postnatal development of electrophysiological properties of principal neurons in the rat basolateral amygdala. J Physiol 590(19):4819–4838CrossRef PubMed PubMedCentral
  Ehrlich DE, Ryan SJ, Hazra R, Guo JD, Rainnie DG (2013) Postnatal maturation of GABAergic transmission in the rat basolateral amygdala. J Neurophysiol 110(4):926–941CrossRef PubMed PubMedCentral
  Elston GN, DeFelipe J (2002) Spine distribution in cortical pyramidal cells: a common organizational principle across species. Prog Brain Res 136:109–133CrossRef PubMed
  Escobar C, Salas M (1993) Neonatal undernutrition and amygdaloid nuclear complex development: an experimental study in the rat. Exp Neurol 122(2):311–318CrossRef PubMed
  Gleich O, Strutz J (2002) Age dependent changes in the medial nucleus of the trapezoid body in gerbils. Hearing Res 164(1–2):166–178CrossRef
  Hubbard DT, Blanchard DC, Yang M, Markham CM, Gervacio A, Chun-I L, Blanchard RJ (2004) Development of defensive behavior and conditioning to cat odor in the rat. Physiol Behav 80(4):525–530CrossRef PubMed
  Hunt PS (1999) A further investigation of the developmental emergence of fear-potentiated startle in rats. Devel Psychobiol 34:281–291CrossRef
  Hunt PS, Richardson R, Campbell BA (1994) Delayed development of fear-potentiated startle in rats. Behav Neurosci 108(1):69–80CrossRef PubMed
  Hunt PS, Hess MF, Campbell BA (1998) Inhibition of the expression of conditioned cardiac responses in the developing rat. Devel Psychobiol 33(3):221–233CrossRef
  Ito W, Pan BX, Yang C, Thakur S, Morozov A (2009) Enhanced generalization of auditory conditioned fear in juvenile mice. Learn Mem 16(3):187–192CrossRef PubMed PubMedCentral
  Johnson SA, Wang JF, Sun X, McEwen BS, Chattarji S, Young LT (2009) Lithium treatment prevents stress-induced dendritic remodeling in the rodent amygdala. Neuroscience 163(1):34–39CrossRef PubMed
  Kaufmann WE, Moser HW (2000) Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 10(10):981–991CrossRef PubMed
  Kim JH, Richardson R (2007) A developmental dissociation in reinstatement of an extinguished fear response in rats. Neurobiol Learn Mem 88(1):48–57CrossRef PubMed
  Kim JH, Richardson R (2008) 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 28(6):1282–1290CrossRef PubMed
  Kim-Cohen J, Caspi A, Moffitt TE, Harrington HL, Milne BJ, Poulton R (2003) Prior juvenile diagnoses in adults with mental disorder: developmental follow-back of a prospective-longitudinal cohort. Arch Gen Psych 60(7):709–717CrossRef
  King EC, Pattwell SS, Glatt CE, Lee FS (2013) Sensitive periods in fear learning and memory. Stress 17(1):13–21CrossRef PubMed PubMedCentral
  Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharm 35(1):217–238CrossRef
  Langton JM, Kim JH, Nicholas J, Richardson R (2007) The effect of the NMDA receptor antagonist MK-801 on the acquisition and extinction of learned fear in the developing rat. Learn Mem 14:665–668CrossRef PubMed
  LeDoux JE (2007) The amygdala. Curr Biol 17(20):R868–R874CrossRef PubMed
  Lee KF, Soares C, Béïque JC (2012) Examining form and function of dendritic spines. Neural Plast 2012:704103PubMed PubMedCentral
  Li C, Dabrowska J, Hazra R, Rainnie DG (2011) Synergistic activation of dopamine D1 and TrkB receptors mediate gain control of synaptic plasticity in the basolateral amygdala. PLoS ONE 6(10):e26065CrossRef PubMed PubMedCentral
  Liao CC, Lee LJ (2012) Evidence for structural and functional changes of subplate neurons in developing rat barrel cortex. Brain Struct Funct 217(2):275–292CrossRef PubMed
  Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382(6589):363–366CrossRef PubMed
  Maren S (2005) Synaptic mechanisms of associative memory in the amygdala. Neuron 47(6):783–786CrossRef PubMed
  McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55(3):257–332CrossRef PubMed
  McEwen BS (2003) Early life influences on life-long patterns of behavior and health. Ment Retard Dev D R 9(3):149–154CrossRef
  Mizukawa K, Tseng IM, 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. Brain Res Dev Brain Res 50(2):197–203CrossRef PubMed
  Monteiro RA, Henrique RM, Rocha E, Marini-Abreu MM, Oliveira MH, Silva MW (1998) Age-related changes in the volume of somata and organelles of cerebellar granule cells. Neurobiol Aging 19(4):325–332CrossRef PubMed
  Monteiro RA, Henrique RM, Oliveira MH, Silva MW, Rocha E (2005) Postnatal cerebellar granule cells of the white rat (rattus norvegicus): a quantitative study, using design-based stereology. Ann Anat 187(2):161–173CrossRef PubMed
  Moriceau S, Roth TL, Okotoghaide T, Sullivan RM (2004) Corticosterone controls the developmental emergence of fear and amygdala function to predator odors in infant rat pups. Int J Dev Neurosci 22:415–422CrossRef PubMed PubMedCentral
  Moryś J, Berdel B, Kowiański P, Dziewiatkowski J (1998) The pattern of synaptophysin changes during the maturation of the amygdaloid body and hippocampal hilus in the rat. Folia Neuropathol 36(1):15–23PubMed
  Moye TB, Rudy JW (1987) Ontogenesis of trace conditioning in young rats: dissociation of associative and memory processes. Dev Psychobiol 20(4):405–414CrossRef PubMed
  Muller JF, Mascagni F, McDonald AJ (2009) Dopaminergic innervation of pyramidal cells in the rat basolateral amygdala. Brain Struct Funct 213(3):275–288CrossRef PubMed
  Muly EC, Senyuz M, Khan ZU, Guo JD, Hazra R, Rainnie DG (2009) Distribution of D1 and D5 dopamine receptors in the primate and rat basolateral amygdala. Brain Struct Funct 213(4–5):375–393CrossRef PubMed PubMedCentral
  Padival MA, Blume SR, Rosenkranz JA (2013) Repeated restraint stress exerts different impact on structure of neurons in the lateral and basal nuclei of the amygdala. Neurosci 246:230–242CrossRef
  Pape HC, Pare D (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90(2):419CrossRef PubMed PubMedCentral
  Pattwell SS, Bath KG, Casey BJ, Ninan I, Lee FS (2011) Selective early-acquired fear memories undergo temporary suppression during adolescence. Proc Natl Acad Sci USA 108(3):1182–1187CrossRef PubMed PubMedCentral
  Pattwell SS, Duhoux S, Hartley CA, Johnson DC, Jing D, Elliott MD, Ruberry EJ, Powers A, Mehta N, Yang RR, Soliman F, Glatt CE, Casey BJ, Ninan I, Lee FS (2012) Altered fear learning across development in both mouse and human. Proc Natl Acad Sci USA 109(40):16318–16323CrossRef PubMed PubMedCentral
  Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, 3rd edn. Academic Press, San Diego
  Pillai AG, de Jong D, Kanatsou S, Krugers H, Knapman A, Heinzmann JM, Holsboer F, Landgraf R, Joëls M, Touma C (2012) Dendritic morphology of hippocampal and amygdalar neurons in adolescent mice is resilient to genetic differences in stress reactivity. PLoS ONE 7(6):e38971CrossRef PubMed PubMedCentral
  Pine DS, Cohen P, Gurley D, Brook J, Ma Y (1998) The risk for early-adulthood anxiety and depressive disorders in adolescents with anxiety and depressive disorders. Arch Gen Psychiatry 55(1):56–64CrossRef PubMed
  Puram SV, Kim AH, Ikeuchi Y, Wilson-Grady JT, Merdes A, Gygi SP, Bonni A (2011) A CaMKIIβ signaling pathway at the centrosome regulates dendrite patterning in the brain. Nat Neurosci 14(8):973–983CrossRef PubMed PubMedCentral
  Quinn R (2005) Comparing rat’s to human’s age: How old is my rat in people years? Nutrition 21(6):775–777CrossRef PubMed
  Raineki C, De Souza MA, Szawka RE, Lutz ML, De Vasconcellos LF, Sanvitto GL, Izquierdo I, Bevilaqua LR, Cammarota M, Lucion AB (2009) Neonatal handling and the maternal odor preference in rat pups: involvement of monoamines and cyclic AMP response element-binding protein pathway in the olfactory bulb. Neuroscience 159(1):31–38CrossRef PubMed
  Rainnie DG (1999) Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82(1):69-85  Rainnie DG, Bergeron R, Sajdyk TJ, Patil M, Gehlert DR, Shekhar A (2004) Corticotrophin releasing factor-induced synaptic plasticity in the amygdala translates stress into emotional disorders. J Neurosci 24(14):3471–3479CrossRef PubMed
  Rainnie DG, Mania I, Mascagni F, McDonald AJ (2006) Physiological and morphological characterization of parvalbumin-containing interneurons in the rat basolateral amygdala. J Comp Neurol 498(1):142–161CrossRef PubMed
  Richardson R, Paxinos G, Lee J (2000) The ontogeny of conditioned odor potentiation of startle. Behav Neurosci 114(6):1167–1173CrossRef PubMed
  Rodrigues SM, Schafe GE, LeDoux JE (2004) Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44(1):75–91CrossRef PubMed
  Romand S, Wang Y, Toledo-Rodriguez M, Markram H (2011) Morphological development of thick-tufted layer v pyramidal cells in the rat somatosensory cortex. Front Neuroanat 5:5CrossRef PubMed PubMedCentral
  Roozendaal B, McEwen BS, Chattarji S (2009) Stress, memory and the amygdala. Nat Rev Neurosci 10(6):423–433CrossRef PubMed
  Rubinow MJ, Drogos LL, Juraska JM (2009) Age-related dendritic hypertrophy and sexual dimorphism in rat basolateral amygdala. Neurobiol Aging 30(1):137–146CrossRef PubMed PubMedCentral
  Rudy JW (1993) Contextual conditioning and auditory cue conditioning dissociate during development. Behav Neurosci 107(5):887–891CrossRef PubMed
  Ryan SJ, Ehrlich DE, Jasnow AM, Daftary S, Madsen TE, Rainnie DG (2012) Spike-timing precision and neuronal synchrony are enhanced by an interaction between synaptic inhibition and membrane oscillations in the amygdala. PLoS ONE 7(4):e35320CrossRef PubMed PubMedCentral
  Shekhar A, Truitt W, Rainnie DG, Sajdyk T (2005) Role of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety. Stress 8(4):209–219CrossRef PubMed
  Shepherd GM (1996) The dendritic spine: a multifunctional integrative unit. J Neurophysiol 75(6):2197–2210PubMed
  Steinberg L (2005) Cognitive and affective development in adolescence. Trends Cogn Sci 9(2):69–74CrossRef PubMed
  Stuber GD, Sparta DR, Stamatakis AM, van Leeuwen WA, Hardjoprajitno JE, Cho S, Tye KM, Kempadoo KA, Zhang F, Deisseroth K, Bonci A (2011) Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475(7356):377–380CrossRef PubMed PubMedCentral
  Sullivan RM, Landers M, Yeaman B, Wilson DA (2000) Good memories of bad events in infancy. Nature 407(6800):38–39CrossRef PubMed
  Takahashi LK (1992) Ontogeny of behavioral inhibition induced by unfamiliar adult male conspecifics in preweanling rats. Physiol Behav 52:493–498CrossRef PubMed
  Thomas CG, Tian H, Diamond JS (2011) The relative roles of diffusion and uptake in clearing synaptically released glutamate change during early postnatal development. J Neurosci 31(12):4743–4754CrossRef PubMed PubMedCentral
  Thompson JV, Sullivan RM, Wilson DA (2008) Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity. Neuroscience 1200:58–65
  Torres-García ME, Solis O, Patricio A, Rodríguez-Moreno A, Camacho-Abrego I, Limón ID, Flores G (2012) Dendritic morphology changes in neurons from the prefrontal cortex, hippocampus and nucleus accumbens in rats after lesion of the thalamic reticular nucleus. Neuroscience 223:429–438CrossRef PubMed
  Tosevski J, Malikovic A, Mojsilovic-Petrovic J, Lackovic V, Peulic M, Sazdanovic P, Alexopulos C (2002) Types of neurons and some dendritic patterns of basolateral amygdala in humans: a golgi study. Ann Anat 184(1):93–103CrossRef PubMed
  Truitt WA, Sajdyk TJ, Dietrich AD, Oberlin B, McDougle CJ, Shekhar A (2007) From anxiety to autism : spectrum of abnormal social behaviors modeled by progressive disruption of inhibitory neuronal function in the basolateral amygdala in Wistar rats. Psychopharmacology 191(1):107–118CrossRef PubMed
  Vidal L, Ruíz C, Villena A, Díaz F, Pérez de Vargas I (2004) Quantitative age-related changes in dorsal lateral geniculate nucleus relay neurons of the rat. Neurosci Res 48(4):387–396CrossRef PubMed
  Wiedenmayer CP, Barr GA (2001) Developmental changes in responsivity to threat are stimulus-specific in rats. Dev Psychobiol 39(1):1–7CrossRef PubMed
  Yajeya J, de la Fuente Juan A, Merchan MA, Riolobos AS, Heredia M, Criado JM (1997) Cholinergic responses of morphologically and electrophysiologically characterized neurons of the basolateral complex in rat amygdala slices. Neuroscience 78(3):731–743CrossRef PubMed
  Zhang ZW (2004) Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. J Neurophysiol 91(3):1171–1182CrossRef PubMed
  Zhang J, Muller JF, McDonald AJ (2013) Noradrenergic innervation of pyramidal cells in the rat basolateral amygdala. Neuroscience 228:395–408CrossRef PubMed PubMedCentral
  
• 作者单位：Steven J. Ryan (1)
  David E. Ehrlich (1)
  Donald G. Rainnie (1)
  
  1. Department of Psychiatry and Behavioral Sciences, Division of Behavioral Neuroscience and Psychiatric Disorders, Yerkes Research Center, Emory University School of Medicine, 954 Gatewood Rd., Atlanta, GA, 30033, USA
  
• 刊物主题：Neurosciences; Cell Biology; Neurology;
• 出版者：Springer Berlin Heidelberg
• ISSN：1863-2661

文摘

The basolateral nucleus of the amygdala (BLA) assigns emotional valence to sensory stimuli, and many amygdala-dependent behaviors undergo marked development during postnatal life. We recently showed principal neurons in the rat BLA undergo dramatic changes to their electrophysiological properties during the first postnatal month, but no study to date has thoroughly characterized changes to morphology or gene expression that may underlie the functional development of this neuronal population. We addressed this knowledge gap with reconstructions of biocytin-filled principal neurons in the rat BLA at postnatal days 7 (P7), 14, 21, 28, and 60. BLA principal neurons underwent a number of morphological changes, including a twofold increase in soma volume from P7 to P21. Dendritic arbors expanded significantly during the first postnatal month and achieved a mature distribution around P28, in terms of total dendritic length and distance from soma. The number of primary dendrites and branch points were consistent with age, but branch points were found farther from the soma in older animals. Dendrites of BLA principal neurons at P7 had few spines, and spine density increased nearly fivefold by P21. Given the concurrent increase in dendritic material, P60 neurons had approximately 17 times as many total spines as P7 neurons. Together, these developmental transitions in BLA principal neuron morphology help explain a number of concomitant electrophysiological changes during a critical period in amygdala development.