Abstract
Our working hypothesis, over the past decade, has been that the limbic system modulates stress ulcer susceptibility1,2. It was largely based on early reports in the literature that linked (in a vague kind of way) this system of interconnected brain structures to the development of so-called “psychosomatic” disorders. In 1949 MacLean3, elaborating on the Papez4 theory of emotions, proposed that the limbic system might represent a primitive “visceral brain”, responsible for the development of psychosomatic diseases. Much of the evidence was based on case reports from patients with temporal lobe epilepsies. Patients with so-called uncinate fits were described, whose feelings of terror were also sometimes associated with visceral auras, i.e., various gastric and intestinal symptoms, ranging from epigastric uneasiness, chewing movements and grinding of the teeth, to feelings of hunger and frequent defecation and urination. Correspondingly, the data from early animal studies indicated that parts of the limbic system might be involved in emotional behavior. Klüver and Bucy5 had reported that monkeys with bilateral temporal lobectomies became tame and docile, showed a collection of symptoms which were labelled “psychic blindness”, displayed various “oral tendencies”, and engaged in bizarre sexual activities. It appeared that the monkeys could no longer discriminate between potentially dangerous objects and objects that might be useful to them. One interpretation of these studies is that the brain lesions had disconnected sensory inputs from the appropriate, adaptive behaviors. Later experiments showed that many of the effects of these radical lobectomies could be traced to damage in the amygdala6. These findings lead to the proposal that the amygdala connects sensory inputs with emotional and visceral responses, based on the recognition that a particular situation may be threatening to the organism7.
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References
P.G. Henke, The hypothalamus-amygdala axis and experimental gastric ulcers, Neurosci Biobehav Rev. 3:75 (1979).
P.G. Henke, The telencephalic limbic system and experimental gastric pathology: A review, Neurosci Biobehav Rev. 6:381 (1982).
P.D. MacLean, Psychosomatic disease and the “visceral brain”: Recent developments bearing on the Papez theory of emotion, Psychosom Med. 11:338 (1949).
J.W. Papez, A proposed mechanism of emotion, Arch Neurol Psychiat. 38:725 (1937).
H. Klüver and P.C. Bucy, Preliminary analysis of functions of the temporal lobes in monkeys, Arch Neurol Psychiat. 42:979 (1934).
G.V. Goddard, Functions of the amygdala, Psychol Bull. 62:87 (1964).
P.G. Henke, The amygdala and forced immobilization of rats, Behav Brain Res. 16:19 (1985).
P.I. Yakovlev, Motility, behavior, and the brain, J Nerv Merit Dis. 107:313 (1948).
J.A. Gray. “The neuropsychology of anxiety,” Oxford University Press, New York (1982).
G. Powell. “Brain and personality,” Praeger Publishers, New York (1979).
M. Bucaille, Electrocoagulations du cerveau préfrontal: Indications et résultats dans les ulcères gastriques et duodénaux rebelles, Acta gastro-enter (belg.). 20:506 (1957).
M. Bucaille, Fontal lobe operation for colitis, Surgery. 52:690 (1962).
R.L. Isaacson. “The limbic system,” Plenum Press, New York (1982).
R.J. Douglas, The development of hippocampal function: Implications for theory and for therapy,in: “The Hippocampus (Vol. 2),” R.L. Isaacson, K.H. Pribram, eds., Plenum Press, New York (1975).
P.G. Henke, Granule cell potentials in the dentate gyrus of the hippocampus: Coping behavior and stress ulcers in rats, Behav Brain Res. 30:97 (1990).
B.R. Kaada, Stimulation and regional ablation of the amygdaloid complex with reference to functional representations, in: “The Neurobiology of the Amygdala,” B.E. Eleftheriou, ed., Plenum Press, New York (1972).
H. Koikegami, Amygdala and other related limbic structures. II. Functional experiments, Acta Med Biol. 12:73 (1964).
P. Gloor, Inputs and outputs of the amygdala: What the amygdala is trying to tell the rest of the brain, in: “Limbic Mechanisms,” K.E. Livingston, D. Hornykiewicz, eds., Plenum Press, New York (1978).
H.J. Lammers, The neural connections of the amygdaloid complex in mammals, in: “The Neurobiology of the Amygdala,” B.E. Eleftheriou, ed., Plenum Press, New York (1972).
J.E. LeDoux, D.A. Ruggiero, and D.J. Reis, Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat, J Comp Neurol. 242:182 (1985).
R. Norgren, Taste pathways to the hypothalamus and amygdala, J Comp Neurol. 166:17 (1976).
O.P. Ottersen and Y. Ben-Ari, Afferent connections to the amygdaloid complex of the rat and cat.I. Projections from the thalamus, J Comp Neurol. 187:401 (1979).
R.J. Radna and P.D. MacLean, Effects of vagal volleys on unit activity of amygdala, hippocampus,and corpus striatum in squirrel monkeys (Saimiri sciureus), Soc Neurosci Abstr. 2:374 (1976).
R.N. Sen and B.K. Anand, Effect of electrical stimulation of the limbic system of brain (“visceral brain”) on gastric secretory activity and ulceration, Indian J Med Res. 45:515 (1957).
C.N. Shealy and T.L. Peele, Studies on amygdaloid nucleus in the cat, J Neurophysiol. 20:125 (1957).
E.J. Zawoisky, Gastric secretory response of the unrestrained cat following electrical stimulation of the hypothalamus, amygdala and basal ganglia, Exp Neurol. 17:128 (1967).
G. Stock, U. Rupprecht, H. Stumpf, and K. Schlör, Cardiovascular changes during arousal elicited by stimulation of amygdala, hypothalamus and locus coeruleus, J Autonom Nerv Syst. 3:503 (1981).
G. Stock, K.H. Schlör, H. Heidt, and J. Buss, Psychomotor behaviour and cardiovascular patterns during stimulation of the amygdala, Pflügers Arch. 376:177 (1978).
R.J. Timms, A study of the amygdaloid defense reaction showing the value of Althesin anesthesia in studies of the functions of the fore-brain in cats, Pflügers Arch. 391:49 (1981).
H.A. Koikegami, A. Komoto, and C. Kido, Studies on the amygdaloid nuclei and periamygdaloid complex: Experiments on the influence of their stimulation upon motility of small intestine and blood pressure, Folia Psychiat Neurol Jap. 7:86 (1953).
S. Eliasson, Cerebral influence on gastric motility in the cat, Acta Physiol Scand. 26 (Suppl. 95):1 (1952).
F.M. Fennegan and M.J. Puiggari, Hypothalamic and amygdaloid influences on gastric motility in dogs, J Neurosurg. 24:497(1966).
P.G. Henke, Recent studies of the central nucleus of the amygdala and stress ulcers, Neurosci Biobehav Rev. 12:143 (1988).
D.L. Innes and M.F. Tansy, Gastric mucosal ulceration associated with electrochemical stimulation of the limbic brain, Brain Res Bull. 5 (Suppl. 1):33 (1980).
P.G. Henke, The centromedial amygdala and gastric pathology in rats, Physiol Behav. 25:107 (1980).
D.A. Hopkins and G. Holstege, Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat, Exp Brain Res. 32:529 (1978).
J.E. Krettek and J.L. Price, Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat, J Comp Neurol. 178:225 (1978).
J.S. Schwaber, B.S. Kapp, G.A. Higgins, and P.R. Rapp, Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus, J Neurosci. 2:1424 (1982).
P.G. Henke, Limbic system modulation of stress ulcer development, Ann NY Acad Sci. 597:201 (1990).
J.L. Price, The efferent projections of the amygdaloid complex in the rat, cat and monkey, in: “The Amygdaloid Complex,” Y. Ben-Ari, ed., Elsevier/North-Holland Biomedical Press, Amsterdam (1981).
P.G. Henke, The amygdala and restraint ulcers in rats, J Comp Physiol Psychol. 84:313 (1980).
P.G. Henke, Facilitation and inhibition of gastric pathology after lesions in the amygdala of rats, Physiol Behav. 25:575 (1980).
P.G. Henke and R.M. Sullivan, Kindling in the amygdala and susceptibility to stress ulcers, Brain Res Bull. 14:5 (1985).
P.G. Henke, Electrophysiological activity in the central nucleus of the amygdala: Emotionality and stress ulcers in rats, Behav Neurosci. 102:77 (1988).
P. Driscoll and K. Bättig, Behavioral, emotional and neurochemical profiles of rats selected for extreme differences in active, two-way avoidance performance, in: “Genetics of the Brain,” I. Lieblich, ed., Elsevier Biomedical Press, Amsterdam (1982).
G. Glavin, Restraint ulcer: History, current research and future implications, Brain Res Bull. 5 (Suppl. 1):51 (1980).
G.B. Glavin and R.E. Ykema, Subject emotionality and subsequent pylorus ligation induced or restraint induced gastric ulcer, Pavlovian J Biol Sci. 15:102 (1980).
A. Ray, P.G. Henke, and R.M. Sullivan, Central dopamine systems and gastric stress pathology in rats, Physiol Behav. 42:359 (1988).
A.Y. Deutsch, M. Goldstein, F. Baldino, and R.H. Roth, Telencephalic projections of the A8 dopamine cell group, Ann NY Acad Sci. 537:27 (1988).
J.H. Fallon, Histochemical characterization of dopaminergic, noradrenergic and serotonergic projections to the amygdala, in: “The Amygdaloid Complex,” Y. Ben-Ari, ed., Elsevier/North-Holland Biomedical Press, Amsterdam (1981).
G.W. Roberts, P.L. Woodham, J.M. Polak, and T.J. Crow, Distribution of neuropeptides in the limbic system of the rat: The amygdaloid complex, Neuroscience. 7:99 (1982).
G.W. Roberts, J.M. Polak, and T.J. Crow, Peptide circuitry of the limbic system, in: “Psychopharmacology of the Limbic System,” M.R. Trimble, E. Zarifian, eds., Oxford University Press, Oxford (1985).
N. Sharif and D. Burt, Limbic, hypothalamic, cortical and spinal regions are enriched with receptors of thyrotropin-releasing hormone: Evidence from [3H] ultrafilm autoradiography and correlation with cerebral effects of the tripeptide in rat brain, Neurosci Lett. 60:337 (1985).
T.H. Williams, M.D. Cassell, N.J. Mankovich, H.K. Huang, and T.S. Gray, The distribution of neuropeptides in the central nucleus of the amygdala: A quantitative approach using image analysis, in: “The Amygdaloid Complex,” Y. Ben-Ari, ed., Elsevier/North-Holland Biomedical Press, Amsterdam (1981).
P.G. Henke, R.M. Sullivan, and A. Ray, Interactions of thyrotropin-releasing hormone with neurotensin and dopamine in the central nucleus of the amygdala during stress ulcer formation in rats, Neurosci Lett. 91:95 (1988).
A. Ray, P.G. Henke, and R.M. Sullivan, The central amygdala and immobilization stress induced gastric pathology in rats: Neurotensin and dopamine, Brain Res. 409:398 (1987).
A. Ray, P.G. Henke, and R.M. Sullivan, Effects of intra- amygdalar dopamine agonists and antagonists on gastric stress lesions in rats, Neurosci Lett. 84:302 (1988).
A. Ray and P.G. Henke, Role of dopaminergic mechanisms in the central amygdalar nucleus in the regulation of stress-induced gastric ulcer formation in rats, Indian J Med Res. 90:224 (1989).
A. Ray, P.G. Henke, and R.M. Sullivan, Opiate mechanisms in the central amygdala and gastric stress pathology in rats, Brain Res. 442:195 (1988).
A. Ray and P.G. Henke, Enkephalin-dopamine interactions in the central amygdalar nucleus during gastric stress ulcer formation in rats, Behav Brain Res. 36:179 (1990).
R.M. Sullivan, P.G. Henke, A. Ray, M.A. Hebert, and J.M. Trimper, The GABA/ benzodiazepine receptor complex in the central amygdalar nucleus and stress ulcers in rats, Beltav Neur Biol. 51:262 (1989).
A. Ray, P.G. Henke, and R.M. Sullivan, Effects of intra-amygdalar thyrotropin releasing hormone (TRH) and its antagonism by atopine and benzodiazepines during stress ulcer formation in rats, Pharmacol Biochem Behav. 36:597 (1990).
D.G. Amaral, J.L. Price, A. Pitkanen, and T.S. Carmichael, Anatomical organization of the primate amygdaloid complex, in: “The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction,” J.P. Aggleton, ed., Wiley-Liss, New York (1992).
E. Costa, M.G. Corda, B. Epstein, C. Forchetti, and A. Guidotti, GABA-benzodiazepine interactions, in: “The Benzodiazepines: From Molecular Biology to Clinical Practice,” E. Costa, ed., Raven Press, New York (1983).
K. Shibata, Y. Kataoka, Y. Gomita, and S. Ueki, Localization of the site of the anticonflict action of benzodiazepines in the amygdaloid nucleus of rats, Brain Res. 234:442 (1982).
K. Nakamura, T. Hayashi, and K. Nakamura, Effects of bromazepam on cerebral neuronal activity in male Wistar rats with immobilized stress, Folia Pharmacol Jap. 83:401 (1984).
P. Gloor, A. Oliver, and L.F. Quesney, The role of the amygdala in the expression of psychic phenomena in temporal lobe seizures, in: “The Amygdaloid Complex,” Y. Ben-Ari, ed., Elsevier/North-Holland Biomedical Press, Amsterdam (1981).
W.P. Chapman, H.R. Schroeder, G. Geyer, M.A.B. Brazier, C. Fager, J.L. Poppen, H.C. Solomon, and P.I. Yakovlev, Physiological evidence concerning the importance of the amygdaloid nuclear region in the integration of circulating function and emotion in man, Science. 129:949 (1954).
CD. Applegate, B.S. Kapp, M.D. Underwood, and C.L. McNall, Autonomic and somatomotor effects of amygdala central n. stimulation in awake rabbits, Physiol Behav. 31:353 (1983).
B.S. Kapp, M. Gallagher, M.D. Underwood, C.L. McNall, and D. Whitehorn, Cardiovascular responses elicited by electrical stimulation of the amygdala central nucleus in the rabbit, Brain Res. 234:251 (1982).
G.J. Mogenson and F.R. Calaresu, Cardiovascular responses to electrical stimulation of the amygdala in the rat, Exp Neurol. 39:166 (1973).
R.M. Harper, R.C. Frysinger, R.B. Trelease, and J.D. Marks, State-dependent alteration of respiratory cycle timing by stimulation of the central nucleus of the amgydala, Brain Res. 306:1 (1984).
J.B. Rosen and M. Davis, Enhancement of acoustic startle by electrical stimulation of the amygdala, Behav Neurosci 102:195 (1988).
P.G. Henke, Unit-activity in the central amygdalar nucleus of rats in response to immobilization stress, Brain Res Bull. 10:833 (1983).
J.P. Pascoe and B.S. Kapp, Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit, Behav Brain Res. 16:117 (1985).
J. Iwata, J.E. LeDoux, M.P. Meeley, S. Arneric, and D J. Reis, Intrinsic neurons in the amygdala field projected to by the medial geniculate body mediate emotional response conditioned to acoustic stimuli, Brain Res. 383:195 (1986).
M.H. Kellicut and J.S. Schwartzbaum, Formation of conditioned emotional response (CER) following lesions of the amygdaloid complex in rats, Psychol Rep. 12:351 (1963).
A.A. Sperack, C.T. Campbell, and L. Drake, Effect of amygdalectomy on habituation and CER in rats, Physiol Behav. 15:199 (1975).
J.M. Hitchcock and M. Davis, Lesions of the amygdala, but not of the cerebellum or red nucleus,block conditioned fear as measured by the potentiated startle paradigm, Behav Neurosci. 100:11 (1986).
C. Kim, H. Choi, J.K. Kim, M.S. Kim, H.J. Park, B.T. Ahn, and S.H. Kang, Influence of hippocampectomy on gastric ulcer in rats, Brain Res. 109:245 (1976).
H.M. Murphy, C.H. Wideman, and T.S. Brown, Plasma corticosterone levels and ulcer formation in rats with hippocampal lesions, Neuroendocrinology. 28:123 (1979).
P.G. Henke, R.J. Savoie, and B.M. Callahan, Hippocampal deafferentation and deefferentation and gastric pathology in rats, Brain Res Bull. 7:395 (1981).
R.A. Nicoll, J.A. Kauer, and R.C. Malenka, The current excitement in long-term potentiation,Neuron. 1:97 (1988).
D.G. Elmes, L.E. Jarrard, and P.D. Swart, Helplessness in hippocampectomized rats: Response perseveration?, Physiol Psychol. 3:51 (1975).
P.G. Henke, Synaptic efficacy in the entorhinal-dentate pathway and stress ulcers in rats, Neurosci Lett. 107:110 (1989).
P.G. Henke, N-methyl-D-aspartate receptors and stress ulcers in rats, in: “Stress and Gastrointestinal Motility,” L. Bueno, ed., John Libbey, London (1989).
P.G. Henke, Potentiation of inputs from the posterolateral amygdala to the dentate gyrus and resistance to stress ulcer formation in rats, Physiol Behav. 48:659 (1990).
P.G. Henke, Effects of naloxone on handling-induced modifications of hippocampal synaptic potentiation and stress ulcers in rats, Exp Clin Gastroenterol. 3:190 (1993).
B.R. Kaada, R.S. Feldman, and T. Langfeldt, Failure to modulate autonomic reflex discharge by hippocampal stimulation in rabbits, Physiol Behav. 7:225 (1971).
P.D. MacLean, Chemical and electrical stimulation of the hippocampus in unrestrained animals,Arch Neurol Psychiat. 81:331(1972).
C.E. Poletti, M. Kliot, and G. Boytin, Metabolic influences of the hippocampus on hypothalamus,preoptic and basal forebrain is exerted through amygdalofugal pathways, Neurosci Lett. 45:211 (1984).
R.E. Adamec and C. Stark-Adamec, Limbic hyperfunction, limbic epilepsy, and interictal behavior:Models and methods of detection, in: “The Limbic System,” B.K. Doane, K.E. Livingston, eds., Raven Press, New York (1986).
P.G. Henke, Hippocampal pathway to the amygdala and stress ulcer development, Brain Res Bull.25:691 (1990).
B.R. Kaada, Cingulate, posterior orbital, anterior insular and temporal pole cortex, in: “Handbook of Physiology, Section 1: Neurophysiology, Vol. 2,” J. Field, H.W. Magoun, V.E. Hall, eds., American Physiological Society, Washington, D.C. (1960).
P.D. MacLean, Culminating developments in the evolution of the limbic system: The thalamocingulate division, in: “The Limbic System,” B.K. Doane, K.E. Livingston, eds., Raven Press, New York (1986).
H.M. Richter, R.A. Davis, D. Ruge, and N.T. Walker, The effect of cortical and subcortical brain lesions upon gastric secretion in dogs with a vagus-preserved total gastric pouch, in: “Surgical Forum, Vol. 7,” American College of Surgeons, Chicago (1956).
E.L. Foltz and L.E. White, Pain “relief” by frontal cingulumotomy, J Neurosurg. 19:89 (1962).
P.G. Henke and R.J. Savoie, The cingulate cortex and gastric pathology, Brain Res Bull. 8:489 (1982).
L.W. Swanson, The anatomical organization of septo-hippocampal projections, in: “Functions of the Septo-Hippocampal System. Ciba Foundation Symposium 58 (new series),” Elsevier, Amsterdam (1978).
P.G. Henke, Mucosal damage following electrical stimulation of the anterior cingulate cortex and pretreatment with atropine and cimetidine, Pharmacol Biochem Behav. 19:483 (1983).
V.B. Domesick, Projections from the cingulate cortex in the rat, Brain Res. 12:296 (1969).
P.G. Henke, The anterior cingulate cortex and stress: Effects of chlordiazepoxide on unit-activity and stimulation-induced gastric pathology in rats, Int J Psychophysiol. 2:23 (1984).
P.G. Henke, R.M. Sullivan, A. Ray, and M.E. MacDougall, Stress ulcer modulation by chlordiazepoxide and GABA in the anterior cingulate cortex of rats, Exp Clin Gastroenterol. 2:13 (1992).
P.G. Henke, Chlordiazepoxide and stress tolerance in rats, Pharmacol Biochem Behav. 26:561 (1987).
R.M. Sullivan and P.G. Henke, The anterior midline cortex and adaptation to stress ulcers in rats,Brain Res Bull. 17:493 (1986).
J.A. Gray, N. Davis, J. Feldon, S. Owen, and M. Boarder, Stress tolerance: Possible neural mechanisms, in: “Foundations of Psychosomatics,” M.J. Christie, P.G. Mellet, eds., John Wiley & Sons, New York (1981).
A. Lenègre, I. Avril, and S. Fromage, Absence of amnesia induction in mice with hydroxyzine in comparison with three other minor tranquillizers, Arzneim Forsch/Drug Res. 38:558 (1988).
M.H. Thiébot, Some evidence for amnesia-like effects of benzodiazepines in animals, Neurosci Biobehav Rev. 9:95 (1985).
K.H. Pribram. “Languages of the Brain,” Prentice-Hall, Englewood Cliffs, N.J. (1971).
D.P. Crowne and D.D. Radcliffe, Some characteristics and functional relations of the electrical activity of the primate hippocampus and a hypothesis of hippocampal function, in: “The Hippocampus, Vol. 2,” R.L. Isaacson, K.H. Pribram, eds., Plenum Press, New York (1975).
J. Olds, The central nervous system and the reinforcement of behavior, Amer Psychol. 24:114 (1969).
B. Milner, S. Corkin, and H.L. Teuber, Further analysis of the hippocampal amnesic syndrome:14-year follow-up study of H. M., Neuropsychologia. 6:215 (1968).
P.G. Henke, A. Ray, and R.M. Sullivan, The amygdala: Emotions and gut functions, Digest Dis Sci. 36:1633 (1991).
P.G. Henke, Stomach pathology and the amygdala, in: “The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction,” J.P. Aggleton, ed., Wiley- Liss, New York (1992).
P.G. Henke and A. Ray, Review: The limbic brain, emotions and stress ulcers, Exp Clin Gastroenterol. 1:287 (1992).
P.G. Henke and A. Ray, Stress ulcer modulation by limbic system structures, Acta Physiol Hung.80:117(1992).
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Henke, P.G. (1995). The Limbic System and Stress Ulcers. In: Szabo, S., Taché, Y., Glavin, G.B. (eds) Neuroendocrinology of Gastrointestinal Ulceration. Hans Selye Symposia on Neuroendocrinology and Stress, vol 2. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1867-9_15
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