Classically conditioned responses following repeated insulin and glucose administration in humans

Behavioural Brain Research

Volumn 110, Issue 1-2, 2000, Pages 143-159

  Stockhorst, Ursula ^a   Steingrüber, Hans Joachim ^a   Scherbaum, Werner A ^b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

Author keywords

Central insulin receptors; Glucose; Hippocampus; Humans; Insulin; Learning; Pavlovian conditioning

Indexed keywords

GLUCOSE; HYDROCORTISONE; INSULIN;

CENTRAL NERVOUS SYSTEM; CONDITIONED REFLEX; CONFERENCE PAPER; ENDOCRINE SYSTEM; GLUCOSE BLOOD LEVEL; HUMAN; HYDROCORTISONE BLOOD LEVEL; INSULIN RELEASE; LEARNING; MEMORY; PRIORITY JOURNAL;

CONDITIONING, CLASSICAL; GLUCOSE; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN;

EID: 0342748441     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-4328(99)00192-8     Document Type: Conference Paper

References (107)

1. Abdallah L., Chabert M., Louis-Sylvestre J. Cephalic phase responses to sweet taste. Am. J. Clin. Nutr. 65:1997;737-743.
2. Alvarez-Buylla R., Carrasco-Zanini J. A conditioned reflex which reproduces the hypoglycemic effect of insulin. Acta Physiol. Latinoamer. 10:1960;153-158.
3. Amir S., Shechter Y. Centrally mediated hypoglycemic effect of insulin: apparent involvement of specific insulin receptors. Brain Res. 418:1987;152-156.
4. Banks W.A., Jaspan J.B., Huang W., Kastin A.J. Transport of insulin across the blood-brain barrier: saturability at euglycemic doses of insulin. Peptides. 18:1997;1423-1429.
5. Baskin D.G., Marks J.L., Schwartz M.W., Figlewicz D.P., Woods S.C., Porte D. Jr. Insulin and insulin receptors in the brain in relation to food intake and body weight. Lehnert H., Murison R., Weiner H., Hellhammer D., Beyer J. Neuronal Control of Bodily Function: Basic and Clinical Aspects. Endocrine and Nutritional Control of Basic Biological Functions. 1993;209-222 Hogrefe & Huber Publishers, vol 7, Seattle.
6. Bellisle F., Louis-Sylvestre J., Demozay F., Blazy D., Le Magnen J. Reflex insulin response associated to food intake in human subjects. Physiol. Behav. 31:1983;515-521.
7. Biessels G.-J., Kamal A., Urban I.J.A., Spruijt B.M., Erkelens D.W., Gispen W.H. Water maze learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: effects of insulin treatment. Brain Res. 800:1998;125-135.
8. Borg M.A., Borg W.P., Tamborlane W.V., Brines M.L., Shulman G.I., Sherwin R.S. Chronic hypoglycemia and diabetes impair counterregulation induced by localized 2-deoxy-glucose perfusion of the ventromedial hypothalamus in rats. Diabetes. 48:1999;584-587.
9. Borg W.P., During M.J., Sherwin R.S., Borg M.A., Brines M.L., Shulman G.I. Ventromedial hypothalamic lesions in rats suppress counterregulatory responses to hypoglycemia. J. Clin. Invest. 93:1994;1677-1682.
10. Borg M.A., Shervin R.S., Borg W.P., Tamborlane W.V., Shulman G.I. Local ventromedial hypothalamus glucose perfusion blocks counterregulation during systemic hypoglycemia in awake rats. J. Clin. Invest. 99:1997;361-365.
11. Broberg D.J., Bernstein I.L. Cephalic insulin release in anorexic women. Physiol. Behav. 45:1989;871-874.
12. Broberg D.J., Bernstein I.L. Preabsorptive insulin release in bulimic women and chronic dieters. Appetite. 13:1989;161-169.
13. Chavez M., Seeley R.J., Green P.K., Wilkinson C.W., Schwartz M.W., Woods S.C. Adrenalectomy increases sensitivity to central insulin. Physiol. Behav. 62:1997;631-634.
14. Chen M., Woods S.C., Porte D. Jr. Effect of cerebral intraventricular insulin on pancreatic insulin secretion in the dog. Diabetes. 24:1975;910-914.
15. Chowers I., Lavy S., Halpern L. Effect of insulin administered intracisternally on the glucose level of the blood and the cerebrospinal fluid in vagotomized dogs. Exp. Neurol. 14:1966;383-389.
16. De Castro J.M., Balagura S. Insulin pretreatment facilitates recovery after dorsal hippocampal lesions. Physiol. Behav. 16:1976;517-520.
17. Deutsch R. Conditioned hypoglycemia: a mechanism for saccharin-induced sensitivity to insulin in the rat. J. Comp. Physiol. Psychol. 95:1974;350-358.
18. Dworkin B.R. Learning and Physiological Regulation. 1993;215 The University of Chicago Press, Chicago.
19. Fehm-Wolfsdorf G., Beermann U., Kern W., Fehm H.L. Failure to obtain classically conditioned hypoglycemia in man. Lehnert H., Murison R., Weiner H., Hellhammer D., Beyer J. Neuronal Control of Bodily Function: Basic and Clinical Aspects. Endocrine and Nutritional Control of Basic Biological Functions. 7:1993;257-261 Hogrefe & Huber Publishers, Seattle.
20. Fehm-Wolfsdorf G., Gnadler M., Kern W., Klosterhalfen W., Kerner W. Classically conditioned changes of blood glucose level in humans. Physiol. Behav. 54:1993;155-160.
21. Fehm-Wolfsdorf G., Pohl J., Kerner W. Classically conditioned changes of blood glucose level in humans. Integr. Physiol. Behav. Sci. 34:1999;132.
22. Flaherty C.F., Becker H.C. Influence of conditioned stimulus context on hyperglycemic conditioned responses. Physiol. Behav. 33:1984;587-593.
23. Flaherty C.F., Becker H.C., Rowan G.A., Voelker S. Effects of chlordiazepoxide on novelty-induced hyperglycemia and on conditioned hyperglycemia. Physiol. Behav. 33:1984;595-599.
24. Flaherty C.F., Grigson P.S., Brady A. Relative novelty of conditioning context influences directionality of glycemic conditioning. J. Exp. Psychol. Anim. Behav. Process. 13:1987;144-149.
25. Flaherty C.F., Rowan G.A., Pohorecky L.A. Corticosterone, novelty-induced hyperglycemia, and chlordiazepoxide. Physiol. Behav. 37:1986;393-396.
26. Flaherty C.F., Uzwiak A.J., Levine J., Smith M., Hall P., Schuler R. Apparent hyperglycemic and hypoglycemic conditioned responses with exogenous insulin as the unconditioned stimulus. Anim. Learn. Behav. 8:1980;382-386.
27. Friedman M.I., Tordoff M.G., Ramirez I. Integrated metabolic control of food intake. Brain Res. Bull. 17:1986;855-859.
28. Goldfine I.D., Abraira C., Gruenewald D., Goldstein M.S. Plasma insulin levels during imaginary food ingestion under hypnosis. Proc. Soc. Exp. Biol. Med. 133:1970;274-276.
29. Grigson P.S., Flaherty C.F. The effect of chlordiazepoxide and propranolol on glycemic conditioning in rats. Psychobiology. 18:1990;422-427.
30. Grill H.J., Berridge K.C., Ganster D.J. Oral glucose is the prime elicitor of preabsorptive insulin secretion. Am. J. Physiol. 246:1984;R88-R95.
31. Havrankova J., Roth J., Brownstein M. Insulin receptors are widely distributed in the central nervous system of the rat. Nature. 272:1978;827-829.
32. Hill J.M., Lesniak M.A., Pert C.B., Roth J. Autoradiographic localization of insulin receptors in rat brain: prominence in olfactory and limbic areas. Neuroscience. 17:1986;1127-1138.
33. Holmes L.J., Smythe G.A., Storlien L.H. Monoaminergic activity at the level of the hypothalamus and striatum: relationship to anticipated feeding and pancreatic insulin responses. Brain Res. 496:1989;204-210.
34. Hopkins D.F.C., Williams G. Insulin receptors are widely distributed in human brain and bind human and porcine insulin with equal affinity. Diabet. Med. 14:1997;1044-1050.
35. Hutton R.A., Woods S.C., Makous W.L. Conditioned hypoglycemia: pseudoconditioning controls. J. Comp. Physiol. Psychol. 71:1970;198-201.
36. Ikeda H., West D.B., Pustek J.J., Figlewicz D.P., Greenwood M.R.C., Porte D. Jr., Woods S.C. Intraventricular insulin reduces food intake and body weight of lean but not obese Zucker rats. Appetite. 7:1986;381-386.
37. Jansen A. The learned nature of binge eating. Legg C.R., Booth D.A. Appetite: Neural and Behavioural Bases. 1994;193-211 Oxford University Press, Oxford.
38. Jansen A., Broekmate J., Heymans M. Cue-exposure vs. self-control in the treatment of binge eating: a pilot study. Behav. Res. Ther. 30:1992;235-241.
39. Johnson W.G., Wildman H.E. Influence of external and covert food stimuli on insulin secretion in obese and normal persons. Behav. Neurosci. 97:1983;1025-1028.
40. Karhunen L.J., Lappalainen R.I., Tammela L., Turpeinen A.K., Uusitupa M.I.J. Subjective and physiological cephalic phase responses to food in obese binge-eating women. Int. J. Eat. Disord. 21:1997;321-328.
41. Karhunen L.J., Lappalainen R.I., Vanninen E.J., Kuikka J.T., Uusitupa M.I.J. Regional cerebral blood flow during food exposure in obese and normal-weight women. Brain. 120:1997;1675-1684.
42. Leibowitz S.F. Hypothalamic neuropeptide Y in relation to energy balance. Ann. NY Acad. Sci. 611:1990;284-301.
43. Levin B.E., Dunn-Meynell A.A., Routh V.H. Brain glucose sensing and body energy homeostasis: role in obesity and diabetes. Am. J. Physiol. 276:1999;R1223-R1231.
44. Lichko A.E. Conditioned reflex hypoglycaemia in man. Pav. J. High. Nerv. Activ. 9:1959;731-737.
45. Louis-Sylvestre J. Preabsorptive insulin release and hypoglycemia in rats. Am. J. Physiol. 230:1976;56-60.
46. Louis-Sylvestre J. Relationship between two stages of prandial insulin release in rats. Am. J. Physiol. 235:1978;E103-E111.
47. Louis-Sylvestre J., Le Magnen J. Palatability and preabsorptive insulin release. Neurosci. Biobehav. Rev. 4:1980;43-46.
48. Lucas F., Bellisle F., Di Maio A. Spontaneous insulin fluctuations and the preabsorptive insulin response to food ingestion in humans. Physiol. Behav. 40:1987;631-636.
49. Matson C.A., Ritter R.C. Long-term CCK-leptin synergy suggests a role for CCK in the regulation of body weight. Am. J. Physiol. 276:1999;R1038-1045.
50. Matysiak J., Green L. On the directionality of classically-conditioned glycemic responses. Physiol. Behav. 32:1984;5-9.
51. Mayer G., Nitsch R., Hoyer S. Effects of changes in peripheral and cerebral glucose metabolism on locomotor activity, learning and memory in adult male rats. Brain Res. 532:1990;95-100.
52. McGowan M.K., Andrews K.M., Kelly J., Grossman S.P. Effects of chronic intrahypothalamic infusion of insulin on food intake and diurnal meal patterning in the rat. Behav. Neurosci. 104:1990;373-385.
53. Mityushov M.I. Conditioned reflex secretion of insulin. Pav. J. High. Nerv. Activ. 4:1954;206-212.
54. Morrell E.M., Surwit R.S., Kuhn C.M., Feinglos M.N., Cochrane C. Classically conditioned enhancement of hyperinsulinemia in the ob/ob mouse. Psychosom. Med. 50:1988;586-590.
55. Moyer A., Rodin J., Cummings N. Cephalic phase insulin release in bulimia. Int. J. Eat. Disord. 14:1993;331-339.
56. Niijima A. Nervous regulation of metabolism. Prog. Neurobiol. 33:1989;135-147.
57. Niijima A., Kannan H., Yamashita H. Neural control of blood glucose homeostasis; effect of microinjection of glucose into hypothalamic nuclei on efferent activity of pancreatic branch of vagus nerve in the rat. Brain Res. Bull. 20:1988;811-815.
58. Oomura Y., Ono T., Ooyama H., Wayner M.J. Glucose and osmosensitive neurones of the rat hypothalamus. Nature. 222:1969;282-284.
59. Overduin J., Dworkin B.R., Jansen A. Introduction and commentary to: M.I. Mityushov, Conditioned reflex secretion of insulin. Integr. Physiol. Behav. Sci. 32:1997;228-246.
60. Overduin J., Jansen A. Conditioned insulin and blood sugar responses in humans in relation to binge eating. Physiol. Behav. 61:1997;569-575.
61. Plaschke K., Hoyer S. Action of the diabetogenic drug streptozotocin on glycolytic and glycogenolytic metabolism in adult rat brain cortex and hippocampus. Int. J. Dev. Neurosci. 11:1993;477-483.
62. Porte D. Jr., Seeley R.J., Woods S.C., Baskin D.G., Figlewicz D.P., Schwartz M.W. Obesity, diabetes and the central nervous system. Diabetologia. 41:1998;863-881.
63. Porte D. Jr., Woods S.C. Neural regulation of islet hormones and its role in energy balance and stress hyperglycemia. Rifkin H., Porte D. Diabetes Mellitus. 1990;175-197 Elsevier, New York.
64. Powley T.L., Berthoud H.R. Diet and cephalic phase insulin responses. Am. J. Clin. Nutr. 42:1985;991-1002.
65. Ramsay D.S., Woods S.C. Biological consequences of drug administration: implications for acute and chronic tolerance. Psychol. Rev. 104:1997;170-193.
66. Reiss W.J. Conditioning of a hyperinsulin type of behavior in the white rat. J. Comp. Physiol. Psychol. 51:1958;301-303.
67. Riedy C.A., Chavez M., Figlewicz D.P., Woods S.C. Central insulin enhances sensitivity to cholecystokinin. Physiol. Behav. 58:1995;755-760.
68. Ritter S., Murnane J.M., Ladenheim E.E. Glucoprivic feeding is impaired by lateral or fourth ventricular alloxan injection. Am. J. Physiol. 243:1982;R312-R317.
69. Roozendaal B., Oldenburger W.P., Strubbe J.H., Koolhaas J.M., Bohus B. The central amygdala is involved in the conditioned but not in the meal-induced cephalic insulin response in the rat. Neurosci. Lett. 116:1990;210-215.
70. Russek M., Piña S. Conditioning of adrenalin anorexia. Nature. 193:1962;1296-1297.
71. Scheurink A.J.W., Balkan B., Nyakas C., van Dijk G., Steffens A.B., Bohus B. Energy homeostasis, autonomic activity and obesity. Obes. Res. 3:1995;721-727.
72. Schwartz M.W., Figlewicz D.P., Baskin D.G., Woods S.C., Porte D. Jr. Insulin in the brain: a hormonal regulator of energy balance. Endocr. Rev. 13:1992;387-414.
73. Schwartz M.W., Figlewicz D.P., Woods S.C., Porte D. Jr., Baskin D.G. Insulin, neuropeptide Y, and food intake. Ann. NY Acad. Sci. 692:1993;60-71.
74. Siegel S. Conditioning of insulin-induced glycemia. J. Comp. Physiol. Psychol. 78:1972;233-241.
75. Siegel S. Conditioning insulin effects. J. Comp. Physiol. Psychol. 89:1975;189-199.
76. Simon C., Schlienger J.L., Sapin R., Imler M. Cephalic phase insulin secretion in relation to food presentation in normal and overweight subjects. Physiol. Behav. 36:1986;465-469.
77. Sjöström L., Garellick G., Krotkiewski M., Luyckx A. Peripheral insulin in response to the sight and smell of food. Metabolism. 10:1980;901-909.
78. Smythe G.A., Grunstein H.S., Bradshaw J.E., Nicholson M.V., Compton P.J. Relationships between brain noradrenergic activity and blood glucose. Nature. 308:1984;65-67.
79. Stein L.J., Dorsa D.M., Baskin D.G., Figlewicz D.P., Porte D. Jr., Woods S.C. Reduced effect of experimental peripheral hyperinsulinemia to elevate cerebrospinal fluid insulin concentrations of obese Zucker rats. Endocrinology. 121:1987;1611-1615.
80. Stockhorst U., Gritzmann E., Klopp K., Schottenfeld-Naor Y., Hübinger A., Berresheim H.W., Steingrüber H.J., Gries F.A. Classical conditioning of insulin effects in healthy humans. Psychosom. Med. 61:1999;424-435.
81. Strack A.M., Sebastian R.J., Schwartz M.W., Dallmann M.F. Glucocorticoids and insulin: reciprocal signals for energy balance. Am. J. Physiol. 268:1995;R142-R149.
82. Strubbe J.H., Mein C.G. Increased feeding in response to bilateral injection of insulin antibodies in the VMH. Physiol. Behav. 19:1977;309-313.
83. Surwit R.S., McCubbin J.A., Livingston E.G., Feinglos M.N. Classically conditioned hyperglycemia in the obese mouse. Psychosom. Med. 47:1985;565-568.
84. Szabo A.J., Iguchi A., Burleson P.D., Szabo O. Vagotomy or atropine blocks hypoglycemic effect of insulin injected into ventromedial hypothalamic nucleus. Am. J. Physiol. 244:1983;E467-E471.
85. Teff K.L., Devine J., Engelman K. Sweet taste: effect on cephalic phase insulin release in men. Physiol. Behav. 57:1995;1089-1095.
86. Teff K.L., Engelman K. Palatability and dietary restraint: effect on cephalic phase insulin release in women. Physiol. Behav. 60:1996;567-573.
87. Teff K.L., Levin B.E., Engelman K. Oral sensory stimulation in men: effects on insulin, C-peptide, and catecholamines. Am. J. Physiol. 265:1993;R1223-1230.
88. Teff K.L., Mattes R.D., Engelman K. Cephalic phase insulin release in normal weight males: verification and reliability. Am. J. Physiol. 261:1991;E430-E436.
89. Thompson CJ, Baylis PH. Endocrine changes during insulin-induced hypoglycaemia. In: Frier BM, Fisher BM, editors. Hypoglycaemia and Diabetes, London: Edward Arnold, 1993, pp. 116-131.
90. Valenstein E.S., Weber M.L. Potentiation of insulin coma by saccharin. J. Comp. Physiol. Psychol. 60:1965;443-446.
91. Wickelgren I. Tracking insulin to the mind. Science. 280:1998;517-519.
92. Woods S.C. Conditioned hypoglycemia: effect of vagotomy and pharmacological blockade. Am. J. Physiol. 223:1972;1424-1427.
93. Woods S.C. Conditioned hypoglycemia. J. Comp. Physiol. Psychol. 90:1976;1164-1168.
94. Woods S.C. The eating paradox: how we tolerate food. Psychol. Rev. 98:1991;488-505.
95. Woods S.C. Insulin and the brain: a mutual dependency. Prog. Psychobiol. Physiol. Psychol. 16:1995;53-81.
96. Woods S.C., Alexander K.R., Porte D. Jr. Conditioned insulin secretion and hypoglycemia following repeated injections of tolbutamide in rats. Endocrinology. 90:1972;227-231.
97. Woods S.C., Bernstein I.L. Cephalic insulin response as a test for completeness of vagotomy to the pancreas. Physiol. Behav. 24:1980;485-488.
98. Woods S.C., Chavez M., Park C.R., Riedy C., Kaiyala K., Richardson R.D., Figlewicz D.P., Schwartz M.W., Porte D. Jr., Seeley R.J. The evaluation of insulin as a metabolic signal influencing behavior via the brain. Neurosci. Biobehav. Rev. 20:1996;139-144.
99. Woods S.C., Hutton R.A., Makous W. Conditioned insulin secretion in the albino rat (34605). Proc. Soc. Exp. Biol. Med. 133:1970;964-968.
100. Woods S.C., Makous W., Hutton R.A. A new technique for conditioned hypoglycemia. Psychon. Sci. 10:1968;389-390.
101. Woods S., Makous W., Hutton A. Temporal parameters of conditioned hypoglycemia. J. Comp. Physiol. Psychol. 69:1969;301-307.
102. Woods S.C., Porte D. Jr., Bobbioni E., Ionescu E., Sauter J.F., Rohner-Jeanrenaud F., Jeanrenaud B. Insulin: its relationship to the central nervous system and to the control of food intake and body weight. Am. J. Clin. Nutr. 42:1985;1063-1071.
103. Woods SC, Ramsay DS. Pavlovian influences over food and drug intake, Behav. Brain Res. 2000; 110: 175-82.
104. Woods S.C., Seeley R.J., Porte D. Jr., Schwartz M.W. Signals that regulate food intake and energy homeostasis. Science. 280:1998;1378-1383.
105. Woods S.C., Vasselli J.R., Kaestner E., Szakmary G.A., Milburn P., Vitiello M.V. Conditioned insulin secretion and meal feeding in rats. J. Comp. Physiol. Psychol. 91:1977;128-133.
106. Wozniak M., Rydzewski B., Baker S.P., Raizada M.K. The cellular and physiological actions of insulin in the central nervous system. Neurochem. Int. 22:1993;1-10.
107. Zakrzewska K.E., Cusin I., Stricker-Krongrad A., Boss O., Ricquier D., Jeanrenaud B., Rohner-Jeanrenaud F. Induction of obesity and hyperleptinemia by central glucocorticoid infusion in the rat. Diabetes. 48:1999;365-370.