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Inputs and Outputs

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The Amygdaloid Nuclear Complex

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Abstract

The authors state in the first lines of the chapter they can only report literature data. The inputs are studied first (afferent fibres to the amygdala come from the olfactory tract, midbrain, forebrain and brainstem). The outputs are discussed in reference to connection pathways seen in the previous chapter. Also reviewed are the amygdalofugal fibres joining the structures studied in the inputs.

An overview of the amygdala physiology is closing the chapter.

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Notes

  1. 1.

    HT Ghashghaei et al. (2007) also observed projections towards the amygdala, from the lateral prefrontal cortex, but they are much more rare and scattered than those from the orbitofrontal and medial frontal areas. Moreover, these projections go preferentially to the baso-lateral nucleus of the amygdala.

  2. 2.

    The accumbens nucleus receives not only inputs from the amygdala via the stria terminalis but also from hippocampus, via the fimbria (AE Kelley et al. 1982).

  3. 3.

    There are many cortical loops but none of them are as important as the amygdala: This is the case with the punishment pathway, called the PVS, periventricular system, because it involves the thalamus and the hypothalamus (plus the midbrain PAG). It is also the case with the action inhibitor pathway, called the behavioural inhibitory system (BIS), in which the noradrenergic fibres, born from the locus coeruleus, and serotoninergic fibres, born from the median raphe nuclei, are involved.

  4. 4.

    In fMRI, one observes hyperactivation of the right amygdala and hypoactivation of the hippocampus (N Kaouane et al. 2012).

  5. 5.

    Marcel Proust, French author (1871–1922). His primary work is called “La recherche du temps perdu” (In search of lost time) (Prix Goncourt 1919). Volume 1, “Du côté de chez Swann” (Towards at Swan), is the one in which the famous page about the memories of tea and madeleine is written!

  6. 6.

    Deep brain stimulation (DBS) through bilateral implantation of electrodes in the nuclei accumbens has been successfully tested in cases of major depression, extremely resistant to all treatments (Th E Schlaeper et al. 2008).

  7. 7.

    Until recently, the amygdala was considered as the receptacle for only emotions of fear or negative emotions in general. Recent work suggests that it also has a role in the receipt of positive emotions (MG Baxter and EA Murray 2002), and this role may be at least as important as the first one.

  8. 8.

    The intense iterative stimulation of the nucleus accumbens may cause an involution of the striatum such as observed by S Kühn et al. (2014) by fMRI in young men with a habit of watching pornographic videos: The greater the stimulation (assessed in number of hours of video watching/week!), the greater the reduction of the volume of the right caudate nucleus and left putamen.

  9. 9.

    The effect of this emotion related to fear is obvious when you see a child turn his head so as not to look, to huddle with his mother while clutching her mother’s skirt, simply because the mother asked him to say hello to the neighbour she had just met. The apprehension to an unknown face, even though female like his mother! If the mother had the misfortune to add: “this woman is going to look after you for a few hours,… while I go…”, the child’s fear could turn into panic with the fear of being abandoned, and this will involve “I don’t want to” and crying manifestations, negative emotions which are part of the amygdala.

References

  • Izquierdo A, Murray EA (2005) Opposing effects of amygdala and orbital prefrontal cortex lesions on the extinction of instrumental responding in macaque monkeys. Eur J Neurosci 22(9):2341–2346

    Article  PubMed  Google Scholar 

  • Zhang DX, Bertram EH (2002) Midline thalamic region: widespread excitatory input to the entorhinal cortex and amygdala. J Neurosci 22(8):3277–3284

    CAS  PubMed  Google Scholar 

  • Aggleton JP, Burton MJ, Passingham RE (1980) Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulata). Brain Res 190(2):347–368

    Article  CAS  PubMed  Google Scholar 

  • Aggleton JP, Mishkin M (1984) Projections of the amygdala to the thalamus in the cynomolgus monkey. J Comp Neurol 222:56–68

    Article  CAS  PubMed  Google Scholar 

  • Amaral DG, Cowan WM (1980) Subcortical afferents to the hippocampal formation in the monkey. J Comp Neurol 189(4):573–591

    Article  CAS  PubMed  Google Scholar 

  • Amaral DG, Cowan WM (1980) Subcortical afferents to the hippocampal formation in the monkey. J Comp Neurol 189(4):573–591

    Google Scholar 

  • Ball T, Derix J, Wentlandt J, Wieckorst B, Speck O, Schulze-Bonhage A, Mutschler I (2009) Anatomical specificity of functional amygdala imaging of responses to stimuli with positive and negative emotion valence. J Neurosci Methods 180(1):57–70

    Article  PubMed  Google Scholar 

  • Barbas H (2000) Connections underlying the synthesis of cognition memory and emotion in primate prefrontal cortices. Brain Res Bull 52:319–330

    Article  CAS  PubMed  Google Scholar 

  • Barbas H (2000) Connections underlying the synthesis of cognition memory and emotion in primate prefrontal cortices. Brain Res Bull 52:319–330

    Google Scholar 

  • Bauer RM (1982) Visual hypoemotionality as a symptom of visual-limbic disconnection in man. Arch Neurol 39:702–708

    Article  CAS  PubMed  Google Scholar 

  • Bauer RM (1982) Visual hypoemotionality as a symptom of visual-limbic disconnection in man. Arch Neurol 39:702–708

    Google Scholar 

  • Ben-Ari Y (1981) The amygdaloid complex. Proceedings of the international symposium on the amygdaloid complex (Senlis; France: 1–4 Sept 1981). Inserm symposium n°20. Editor: Yehezkel Ben-Ari. Elsevier/North Holland Biomedical Press

    Google Scholar 

  • Ben-Ari Y, Tremblay E (1982) Organization of the amygdala with special reference to various pathological syndromes. Scand J Psychol 23(Suppl 1):26–36

    Article  Google Scholar 

  • Burstein R, Potrebic S (1993) Retrograde labelling of neurons in the spinal cord that project directly to the amygdala or the orbital cortex in the rat. J Comp Neurol 235(4):469–485

    Article  Google Scholar 

  • Canteras NS, Swanson LW (1992) Projections of the ventral subiculum to the amygdala, septum and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J Comp Neurol 324(2):180–194

    Article  CAS  PubMed  Google Scholar 

  • Carmichael ST, Clugnet MC, Price JL (1994) Central olfactory connections in the macaque monkey. J Comp Neurol 346(3):403–434

    Article  CAS  PubMed  Google Scholar 

  • Chang L, Sundaresh S, Elliott J, Anton PA, Baldi P, Licudine A, Mayer M, Vuong T, Hirano M, Naliboff BD, Ameen VZ, Mayer EA (2009) Dysregulation of the hypothalamic-pituitary-adrenal (HPA) axis in irritable bowel syndrome. Neurogastroenterol Motil 21:149–159

    Article  CAS  PubMed  Google Scholar 

  • Cho YT, Ernst M, Fudge JL (2013) Cortico-amygdala-striatal circuits are organized as hierarchical subsystems through the primate amygdala. J Neurosci 33(35):14017–14030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciriello J, Schultz CG, Roder S (1994) Collateral axonal projections from ventrolateral medullary non-catecholaminergic neurons to central nucleus of the amygdala. Brain Res 663(2):346–351

    Article  CAS  PubMed  Google Scholar 

  • Damasio AR (2003) Spinoza avait raison. Joie et tristesse, le cerveau des émotions. Odile Jacob, Paris

    Google Scholar 

  • Damasio AR (2004) L’erreur de Descartes. La raison des émotions. Odile Jacob, Paris

    Google Scholar 

  • Edeline JM, Weinberger NM (1992) Associative retuning in the thalamic source of input to the amygdale and auditory cortex: receptive field plasticity in the medial division of the medial geniculate body. Behav Neurosci 106(1):81–105

    Article  CAS  PubMed  Google Scholar 

  • Fudge JL, Kunishio K, Walsh P, Richard C, Haber SN (2002) Amygdaloid projections to ventromedial striatal subterritories in the primate. Neuroscience 110(2):257–275

    Article  CAS  PubMed  Google Scholar 

  • Ghashghaei HT, Barbas H (2002) Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115(4):1261–1270

    Article  CAS  PubMed  Google Scholar 

  • Ghashghaei HT, Hilgetag CC, Barbas H (2007) Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 34(3):905–923

    Article  CAS  PubMed  Google Scholar 

  • Gray TS, Carney ME, Magnuson DJ (1989) Direct projections from the central amygdala nucleus to the hypothalamic paraventricular nucleus: possible role in stress-induced adrenocorticotropin release. Neuroendocrinology 50(4):433–446

    Article  CAS  PubMed  Google Scholar 

  • Hanaway J, Woolsey TH, Gado MH, Roberts MP (2001) Atlas du Cerveau. De Boeck Université, traduction française par Dhem A

    Google Scholar 

  • Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20(2):78–83

    Article  CAS  PubMed  Google Scholar 

  • Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20(2):78–83

    Google Scholar 

  • Höistad M, Barbas H (2008) Sequence of information processing for emotions through pathways linking temporal and insular cortices with the amygdala. Neuroimage 40(3):1016–1033

    Article  PubMed  PubMed Central  Google Scholar 

  • Holstege G (1991) Descending motor pathways and the spinal motor system: limbic and non limbic components. Prog Brain Res 87:307–412, ch. 4

    Article  CAS  PubMed  Google Scholar 

  • Insausti R, Amaral DG, Cowan WM (1987) The entorhinal cortex of the monkey: III. Subcortical afferents. J Comp Neurol 264(3):396–408

    Article  CAS  PubMed  Google Scholar 

  • Iwai E, Yukie M (1987) Amygdalofugal and amygdalopetal connections with modality-specific visual cortical areas in macaques (Macaca fuscata, M. Mulatta, and M. Fascicularis). J Comp Neurol 261(3):362–387

    Article  CAS  PubMed  Google Scholar 

  • Ji Y, Tang B, Traub RJ (2008) The visceromotor response to colorectal distention fluctuates with the estrous cycle in rats. Neuroscience 154:1562–1567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jongen-Rêlo AL, Amaral DG (1998) Evidence for a GABAergic projection from the central nucleus of the amygdala to the brainstem of the macaque monkey: a combined retrograde tracing and in situ hybridization study. Eur J Neurosci 10(9):2924–2933

    Article  PubMed  Google Scholar 

  • Kaouane N, Porte Y, Vallée M, Brayda-Bruno L, Mons N, Calandreau L, Marighetto A, Piazza PV, Desmedt A (2012) Glucocorticoids can induce PTSD-like memory impairments in mice. Science 335:1510–1513

    Article  CAS  PubMed  Google Scholar 

  • Karama S, Lecours AR, Leroux JM, Bourgouin P, Beaudoin G, Joubert S, Beauregard M (2002) Areas of brain activation in males and females, during viewing of erotic film excerpts. Hum Brain Mapp 16(1):1–13

    Article  PubMed  Google Scholar 

  • Kelley AE, Domesick VB, Nauta WJH (1982) The amygdalostriatal projection in the rat – an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7(3):615–630

    Article  CAS  PubMed  Google Scholar 

  • LeDoux JE (1987) Emotion. In: Fishman AP (ed) Handbook of physiology. 1: The nervous system. American Physiological Society, Bethesda, pp 419–460

    Google Scholar 

  • LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184

    Article  CAS  PubMed  Google Scholar 

  • LeDoux JE, Cicchetti P, Xagoraris A, Romanski L-M (1990a) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10:1062–1069

    CAS  PubMed  Google Scholar 

  • LeDoux JE, Farb C, Ruggiero DA (1990b) Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J Neurosci 10(4):1043–1054

    CAS  PubMed  Google Scholar 

  • Leichnetz GR, Astruc J (1977) The course of some prefrontal corticofugals to the pallidum, substantia innominata, and amygdaloid complex in monkeys. Exp Neurol 54(1):104–109

    Article  CAS  PubMed  Google Scholar 

  • Lenhardt ML, Shulman A, Goldstein BA (2007) The role of the parabrachial nucleus in the natural history of tinnitus and its implications. Int Tinnitus J 13(2):87–89

    PubMed  Google Scholar 

  • McGaugh JL (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27(1):1–28

    Article  CAS  PubMed  Google Scholar 

  • Mehler WR (1980) Subcortical afferent connections of the amygdala in the monkey. J Comp Neurol 190(4):733–762

    Article  CAS  PubMed  Google Scholar 

  • Mizuno N, Takahashi O, Satoda T, Matsushima R (1985) Amygdalospinal projections in the macaque monkey. Neurosci Lett 53(3):327–330

    Article  CAS  PubMed  Google Scholar 

  • Moga MM, Gray TS (1985) Evidence for corticotropin-releasing factor, neurotensin, and somatostatin in the neural pathway from the central nucleus of the amygdala to the parabrachial nucleus. J Comp Neurol 241(3):275–284

    Article  CAS  PubMed  Google Scholar 

  • Morris JS, Frith CD, Perrett DI, Rowland D, Young AW, Calder AJ, Dolan RJ (1996) A differential neural response in the human amygdale to fearful and happy facial expressions. Nature 383:812–815

    Article  CAS  PubMed  Google Scholar 

  • Morris JS, Ohman A, Dolan RJ (1999) A subcortical pathway to the right amygdala mediating “unseen” fear. Proc Natl Acad Sci U S A 96(4):1680–1685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mufson EJ, Mesulam MM, Pandya DN (1981) Insular interconnections with the amygdale in rhesus monkey. Neuroscience 7:1231–1248

    Article  Google Scholar 

  • Mesulam MM, Mufson EJ (1985) The insula of Reil in man and monkey. In: Peters A, Jones EG (eds) Association and auditory cortices, vol 4, Cerebral cortex. Plenum, New York, pp 179–226

    Chapter  Google Scholar 

  • Nauta WJH (1961) Fibre degeneration following lesions of the amygdaloid complex in the monkey. J Anat 95:515–531

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nauta WJH, Haymaker W (1969) Hypothalamic nuclei and fiber connections. In: Haymaker W, Anderson E, Nauta WJH (eds) The hypothalamus. Thomas, Springfield, pp 136–209

    Google Scholar 

  • Nieuwenhuys R, Voogd J, van Huijzen C (2008) The human central nervous system, 4th edn. Springer, New York

    Book  Google Scholar 

  • Norita M, Kawamura K (1980) Subcortical afferents to the monkey amygdala: an HRP study. Brain Res 190(1):225–230

    Article  CAS  PubMed  Google Scholar 

  • Ottersen OP (1980) Afferent connections to the amygdaloid complex of the rat and cat. II. Afferents from the hypothalamus and the basal telencephalon. J Comp Neurol 194:267–289

    Article  CAS  PubMed  Google Scholar 

  • Ottersen OP, Ben-Ari Y (1979) Afferent connections of the amygdaloid complex of the rat and cat. I; afferents from the thalamus. J Comp Neurol 187:401–424

    Article  CAS  PubMed  Google Scholar 

  • Pandya DN, Van Hoesen GW, Domesick VB (1973) A cingulo-amygdaloid projection in the rhesus monkey. Brain Res 61:369–373

    Article  CAS  PubMed  Google Scholar 

  • Petrovich GD (2001) Amygdala (amygdaloid complex). In: International encyclopedia of the social and behavioral sciences. Elsevier, pp 471–473

    Google Scholar 

  • Phelps EA (2004) Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 14(2):198–202

    Article  CAS  PubMed  Google Scholar 

  • Pitkänen A, Pikkarainen M, Nurminen N, Ylinen A (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and posterorhinal cortex in rat. A review. Ann N Y Acad Sci 911:369–391

    Article  PubMed  Google Scholar 

  • Powell TPS, Cowan WM, Raisman G (1965) The central olfactory connexions. J Anat 99:791–813

    CAS  PubMed  PubMed Central  Google Scholar 

  • Price JL, Amaral DG (1981) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1(11):1242–1259

    CAS  PubMed  Google Scholar 

  • Roozendaal B, McEwen BS, Chattarji S (2009) Stress, memory and the amygdala. Nat Rev Neurosci 10:423–433

    Article  CAS  PubMed  Google Scholar 

  • Rosene DL, Van Hoesen GW (1977) Hippocampal efferents reach widespread areas of the cerebral cortex and amygdala in the rhesus monkey. Science 198(4314):315–317

    Article  CAS  PubMed  Google Scholar 

  • Russchen FT, Amaral DG, Price JL (1985a) The afferent connections of the substantia innominata in the monkey, Macaca fascicularis. J Comp Neurol 242(1):1–27

    Article  CAS  PubMed  Google Scholar 

  • Russchen FT, Bakst J, Amaral DG, Price JL (1985b) The amygdalostriatal projections in the monkey. An anterograde tracing study. Brain Res 329(1–2):241–257

    Article  CAS  PubMed  Google Scholar 

  • Salu Y (2013) The role of the amygdala in the development of sexual arousal. Electron J Human Sex 16:1–6

    Google Scholar 

  • Schwaber JS, Kapp BS, Higgins G (1980) The origin and extent of direct amygdala projections to the region of the dorsal motor nucleus of the vagus and the nucleus of the solitary tract. Neurosci Lett 20(1):15–20

    Article  CAS  PubMed  Google Scholar 

  • Stefanacci L, Amaral DG (2000) Topographic organization of cortical inputs to the lateral nucleus of the macaque monkey amygdala: a retrograde tracing study. J Comp Neurol 421(1):52–79

    Article  CAS  PubMed  Google Scholar 

  • Stefanacci L, Amaral DG (2002) Some observations on cortical inputs to the macaque monkey amygdala: an anterograde tracing study. J Comp Neurol 451(4):301–323

    Article  PubMed  Google Scholar 

  • Sundaram T, Jeong GW, Kim TH, Kim GW, Baek HS, Kang HK (2010) Time-course analysis of the neuroanatomical correlates of sexual arousal evoked by erotic video stimuli in healthy males. Korean J Radiol 11(3):278–285

    Article  PubMed  PubMed Central  Google Scholar 

  • Turner BH, Mishkin M, Knapp M (1980) Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. J Comp Neurol 191(4):515–543

    Article  CAS  PubMed  Google Scholar 

  • Soudry Y, Lemogne C, Malinvaud D, Consoli SM, Bonfils P (2011) Olfactory system and emotions: common substrates. Eur Ann Otorhinolaryngol Head Neck Dis 128(1):18–23

    Article  CAS  PubMed  Google Scholar 

  • Van Stegeren AH, Goekoop R, Everaerd W, Scheltens P, Barkhof F, Kuijer JP, Rombouts SA (2005) Noradrenaline mediates amygdala activation in men and women during encoding of emotional material. Neuroimage 24(3):898–909

    Article  PubMed  Google Scholar 

  • Van Hoesen GW (1985) Neural systems of the non-human primate forebrain implicated in memory. Ann N Y Acad Sci 444:97–112

    Article  PubMed  Google Scholar 

  • Veening JG, Swanson LW, Sawchenko PE (1984) The organization of projections from the central nucleus of the amygdale to brainstem sites involved in central autonomic regulation: a combined retrograde transport-immunohistochemical study. Brain Res 303(2):337–357

    Article  CAS  PubMed  Google Scholar 

  • Webster MJ, Lingerleider LG, Bachevalier J (1991) Connections of inferior temporal areas TE and TEO with medial temporal-lobes structures in infant and adult-monkeys. J Neurosci 11(4):1095–1116

    CAS  PubMed  Google Scholar 

  • Wilder-Smith C, Schindler D, Lovblad K, Redmond S, Nirkko A (2004) Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls. Gut 53:1595–1601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuasa S (2009) Somatotopy in the emotional expression by the amygdala. Brain Nerve 61(12):1395–1404

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Faculté de Médecine, Marseille, France

    Vincent Di Marino

  2. Unité de Médecine Légale, Hôpital de la Timone, Marseille, France

    Yves Etienne

  3. Unité SAMU 13, Centre 15, Hôpital de la Timone, Marseille, France

    Maurice Niddam

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  1. Vincent Di Marino
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  2. Yves Etienne
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Di Marino, V., Etienne, Y., Niddam, M. (2016). Inputs and Outputs. In: The Amygdaloid Nuclear Complex. Springer, Cham. https://doi.org/10.1007/978-3-319-23243-0_8

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