Glucose administration enhances fMRI brain activation and connectivity related to episodic memory encoding for neutral and emotional stimuli

Neuropsychologia

Volumn 49, Issue 5, 2011, Pages 1052-1066

  Parent, Marise B ^a   Krebs Kraft, Desiree L ^a   Ryan, John P ^a   Wilson, Jennifer S ^b   Harenski, Carla ^c   Hamann, Stephan ^b  

^a GEORGIA STATE UNIVERSITY   (United States)

^b EMORY UNIVERSITY   (United States)

^c MIND RESEARCH NETWORK   (United States)

Author keywords

Amygdala; Functional connectivity; Hippocampus; Prefrontal cortex

Indexed keywords

GLUCOSE; SACCHARIN;

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; EMOTION; EPISODIC MEMORY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; PATTERN RECOGNITION; PREFRONTAL CORTEX; RECALL; STIMULUS RESPONSE; VISUAL STIMULATION;

ADULT; BLOOD GLUCOSE; BRAIN; BRAIN MAPPING; EMOTIONS; FEMALE; FUNCTIONAL LATERALITY; GLUCOSE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MENTAL RECALL; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PHOTIC STIMULATION; YOUNG ADULT;

EID: 79954417986     PISSN: 00283932     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2011.02.013     Document Type: Article

References (101)

1. Abe K., Fujimoto T., Akaishi T., Misawa M. Basolateral amygdala D1- and D2-dopaminergic system promotes the formation of long-term potentiation in the dentate gyrus of anesthetized rats. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2009, 33(3):552-556.
2. Almaguer-Melian W., Cruz-Aguado R., Riva C.D.L., Kendrick K.M., Frey J.U., Bergado J. Effect of LTP-reinforcing paradigms on neurotransmitter release in the dentate gyrus of young and aged rats. Biochemical and Biophysical Research Communications 2005, 327(3):877-883.
3. Ashburner J., Friston K.J. Nonlinear spatial normalization using basis functions. Human Brain Mapping 1999, 7(4):254-266.
4. Barros L.F., Porras O.H., Bittner C.X. Why glucose transport in the brain matters for PET. Trends in Neuroscience 2005, 28:117-119.
5. Bergado J.A., Frey S., López J., Almaguer-Melian W., Frey J.U. Cholinergic afferents to the locus coeruleus and noradrenergic afferents to the medial septum mediate LTP-reinforcement in the dentate gyrus by stimulation of the amygdala. Neurobiology of Learning and Memory 2007, 88(3):331-341.
6. Benton D. The impact of the supply of glucose to the brain on mood and memory. Nutrition Reviews 2001, 59(1 Pt 2):S20-21.
7. Blake T.M., Varnhagen C.K., Parent M.B. Emotionally arousing pictures increase blood glucose levels and enhance recall. Neurobiology of Learning and Memory 1986, 75(3):262-273.
8. Brandt K.R., Sunram-Lea S.I., Jenkinson P.M., Jones E. The effects of glucose dose and dual-task performance on memory for emotional material. Behavioural Brain Research 2010, 211(1):83-88.
9. Brandt K.R., Sünram-Lea S.I., Qualtrough K. The effect of glucose administration on the emotional enhancement effect in recognition memory. Biological Psychology 2006, 73(2):199-208.
10. Calandreau L., Trifilieff P., Mons N., Costes L., Marien M., Marighetto A., et al. Extracellular hippocampal acetylcholine level controls amygdala function and promotes adaptive conditioned emotional response. Journal of Neuroscience 2006, 26(52):13556-13566.
11. Canal C.E., Stutz S.J., Gold P.E. Glucose injections into the dorsal hippocampus or dorsolateral striatum of rats prior to T-maze training: Modulation of learning rates and strategy selection. Learning and Memory 2005, 12(4):367-374.
12. Choeiri C., Staines W., Miki T., Seino S., Messier C. Glucose transporter plasticity during memory processing. Neuroscience 2005, 130:591-600.
13. Craft S., Murphy C., Wemstrom J. Glucose effects on complex memory and nonmemory tasks: The influence of age, sex, and glucoregulatory response. Psychobiology 1994, 22(2):95-105.
14. Dash P.K., Orsi S.A., Moore A.N. Spatial memory formation and memory-enhancing effect of glucose involves activation of the tuberous sclerosis complex-Mammalian target of rapamycin pathway. Journal of Neuroscience 2006, 26(31):8048-8056.
15. Degroot A., Kornecook T., Quirion R., DeBow S., Parent M.B. Glucose increases hippocampal extracellular acetylcholine levels upon activation of septal GABA receptors. Brain Research 2003, 979:71-77.
16. Durkin T.P., Messier C., de Boer P., Westerink B.H.C. Raised glucose levels enhance scopolamine-induced acetylcholine overflow from the hippocampus: An in vivo microdialysis study in the rat. Behavioural Brain Research 1992, 49(2):181-188.
17. Eichenbaum H., Yonelinas A.P., Ranganath C. The medial temporal lobe and recognition memory. Annual Review of Neuroscience 2007, 30:123-152.
18. Fioramonti X., Lorsignol A., Taupignon A., Penicaud L. A new ATP-sensitive K+ channel-independent mechanism is involved in glucose-excited neurons of mouse arcuate nucleus. Diabetes 2004, 53:2767-2775.
19. Ford C.E., Scholey A.B., Ayre G., Wesnes K. The effect of glucose administration and the emotional content of words on heart rate and memory. Journal of Psychopharmacology 2002, 16(3):241-244.
20. Foster J.K., Lidder P.G., Sunram S.I. Glucose and memory: Fractionation of enhancement effects?. Psychopharmacology 1998, 137(3):259-270.
21. Fox M.D., Zhang D., Snyder A.Z., Raichle M.E. The global signal and observed anticorrelated resting state brain networks. Journal of Neurophysiology 2009, 101(6):3270-3283.
22. Frey S., Bergado-Rosado J., Seidenbecher T., Pape H.-C., Frey J.U. Reinforcement of early long-term potentiation (Early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: Heterosynaptic induction mechanisms of late-LTP. Journal of Neuroscience 2001, 21(10):3697-3703.
23. Friston K.J., Glaser D.E., Henson R.N.A., Kiebel C. Classical and Bayesian inference in neuroimaging. Neuroimage 2002, 16:484-512.
24. Gabrieli J.D., Brewer J.B., Desmond J.E., Glover G.H. Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science 1997, 276(5310):264-266.
25. Gage F.H., Kelly P.A., Bjorklund A. Regional changes in brain glucose metabolism reflect cognitive impairments in aged rats. Journal of Neuroscience 1984, 4:2856-2865.
26. Gerber J.C., Choki J., Brunswick D.J., Reivich M., Frazer A. The effect of antidepressant drugs on regional cerebral glucose utilization in the rat. Brain Research 1983, 269:319-325.
27. Gibbs M.E., Summers R.J. Effects of glucose and 2-deoxyglucose on memory formation in the chick: Interaction with beta(3)-adrenoceptor agonists. Neuroscience 2002, 114(1):69-79.
28. Gold P.E. Glucose modulation of memory storage processing. Behavioral and Neural Biology 1986, 45(3):342-349.
29. Gold P.E. Coordination of multiple memory systems. Neurobiology of Learning and Memory 2004, 82(3):230-242.
30. Gold P.E., Vogt J., Hall J.L. Glucose effects on memory: behavioral and pharmacological characteristics. Behavioral and Neural Biology 1986, 46:145-155.
31. Gore J.B., Krebs D.L., Parent M.B. Changes in blood glucose and salivary cortisol are not necessary for arousal to enhance memory in young or older adults. Psychoneuroendocrinology 2006, 31(5):589-600.
32. Gruetter R., Ugurbil K., Seaquist E.R. Effect of acute hyperglycemia on visual cortical activation as measured by functional MRI. Journal of Neuroscience Research 2000, 62:279-285.
33. Hale P.J., Wright J.V., Nattrass M. Differences in insulin sensitivity between normal men and women. Metabolism: Clinical and Experimental 1985, 34(12):1133-1138.
34. Hamann S. Cognitive and neural mechanisms of emotional memory. Trends in Cognitive Sciences 2001, 5(9):394-400.
35. Holmes A.P., Friston K.J. Generalisability, random effects and population inference. Neuroimage 1998, 7:S754.
36. Holmes A.P., Josephs O., Buchel C., Friston K.J. Statistical modelling of low-frequency confounds in fMRI. Proceedings of the 3rd international conference on functional mapping of the human brain 1997, S480.
37. Kennedy D.O., Scholey A.B. Glucose administration, heart rate and cognitive performance: Effects of increasing mental effort. Psychopharmacology 2000, 149(1):63-71.
38. Kensinger E.A., Corkin S. Memory enhancement for emotional words: Are emotional words more vividly remembered than neutral words?. Memory and Cognition 2003, 31(8):1169-1180.
39. Khandelwal P., Beyer C.E., Lin Q., McGonigle P., Schechter L.E., Bach A.C. Nanoprobe NMR spectroscopy and in vivo microdialysis: new analytical methods to study brain neurochemistry. Journal of Neuroscience Methods 2004, 133:181-189.
40. Kimbrell T.A., Dunn R.T., George M.S., Danielson A.L., Willis M.W., Repella J.D., et al. Left prefrontal-repetitive transcranial magnetic stimulation (rTMS) and regional cerebral glucose metabolism in normal volunteers. Psychiatry Research 2002, 115:101-113.
41. Kopf S.R., Baratti C.M. Memory-improving actions of glucose: Involvement of a central cholinergic muscarinic mechanism. Behavioral and Neural Biology 1994, 62(3):237-243.
42. Korol D.L., Gold P.E. Glucose, memory, and aging. American Journal of Clinical Nutrition 1998, 67(4):764S-771S.
43. Korol D.L., Lexcen F.J., Parent M., Ragozzino M.E., Manning C.A., Gold P.E. Effects of glucose on cognitive performance in college students. Soc Neurosci Abstr 1995, 21:2085.
44. Korz V., Frey J.U. Bidirectional modulation of hippocampal long-term potentiation under stress and no-stress conditions in basolateral amygdala-lesioned and intact rats. Journal of Neuroscience 2005, 25(32):7393-7400.
45. Krebs-Kraft D.L., Parent M.B. Hippocampal infusions of glucose reverse memory deficits produced by co-infusions of a GABA receptor agonist. Neurobiology of Learning and Memory 2008, 89(2):142-152.
46. LaBar K.S., Cabeza R. Cognitive neuroscience of emotional memory. Nature Reviews Neuroscience 2006, 7(1):54-64.
47. Lang P.J., Bradley M.M., Cuthbert B.N. International affective picture system (IAPS): Affective ratings of pictures and instruction manual 2008, University of Florida, Gainesville, FL.
48. Lee M.K., Graham S.N., Gold P.E. Memory enhancement with posttraining intraventricular glucose injections in rats. Behavioral Neuroscience 1988, 102(4):591-595.
49. Liu Y., Gao J.H., Liu H.L., Fox P.T. The temporal response of the brain after eating revealed by functional MRI. Nature 2000, 405(6790):1058-1062.
50. Mahankali S., Liu Y., Pu Y., Wang J., Chen C.W., Fox P.T., et al. In vivo fMRI demonstration of hypothalamic function following intraperitoneal glucose administration in a rat model. Magnetic Resonance in Medicine 2000, 43(1):155-159.
51. Manning C.A., Ragozzino M.E., Gold P.E. Glucose enhancement of memory in patients with probable senile dementia of the Alzheimer's type. Neurobiology of Aging 1993, 14(6):523-528.
52. Manning C.A., Stone W.S., Korol D.L., Gold P.E. Glucose enhancement of 24-h memory retrieval in healthy elderly humans. Behavioural Brain Research 1998, 93(1-2):71-76.
53. Mazaika, P., Whitfield-Gabrieli, S., & Reiss, A. (2007). Artifact repair for fMRI data from high motion clinical subjects. Paper presented at the Human Brain Mapping.
54. McGaugh J.L., Cahill L., Roozendaal B. Involvement of the amygdala in memory storage: Interaction with other brain systems. Proceedings of the National Academy of Sciences of the United States of America 1996, 93(24):13508-13514.
55. McNay E.C., Fries T.M., Gold P.E. Decreases in rat extracellular hippocampal glucose concentration associated with cognitive demand during a spatial task. Proceedings of the National Academy of Sciences of the United States of America 2000, 97(6):2881-2885.
56. McNay E.C., Gold P.E. Memory modulation across neural systems: Intra-amygdala glucose reverses deficits caused by intraseptal morphine on a spatial task but not on an aversive task. Journal of Neuroscience 1998, 18(10):3853-3858.
57. Meikle A., Riby L.M., Stollery B. The impact of glucose ingestion and gluco-regulatory control on cognitive performance: A comparison of younger and middle aged adults. Human Psychopharmacology 2004, 19(8):523-535.
58. Messier C. Glucose improvement of memory: A review. European Journal of Pharmacology 2004, 490(1-3):33-57.
59. Messier C., Tsiakas M., Gagnon M., Desrochers A., Awad N. Effect of age and glucoregulation on cognitive performance. Neurobiology of Aging 2003, 24(7):985-1003.
60. Messier C., White N.M. Memory improvement by glucose, fructose, and two glucose analogs: A possible effect on peripheral glucose transport. Behavioral and Neural Biology 1987, 48(1):104-127.
61. Metzger M.M., Flint R.W. Glucose enhancement of face recognition is unaffected by alterations of face features. Neurobiology of Learning and Memory 2003, 80(2):172-175.
62. Mohanty A., Flint R.W. Differential effects of glucose on modulation of emotional and nonemotional spatial memory tasks. Cognitive, Affective, & Behavioral Neuroscience 2001, 1(1):90-95.
63. Nakao K., Matsuyama K., Matsuki N., Ikegaya Y. Amygdala stimulation modulates hippocampal synaptic plasticity. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(39):14270-14275.
64. Paller K.A., Kutas M., Mayes A.R. Neural correlates of encoding in an incidental learning paradigm. Electroencephalography and Clinical Neurophysiology 1987, 67(4):360-371.
65. Pardridge W.M., Boado R.J., Farrell C.R. Brain-type glucose transporter (GLUT-1) is selectively localized to the blood-brain barrier. Studies with quantitative western blotting and in situ hybridization. The Journal of Biological Chemistry 1990, 265(29):18035-18040.
66. Parent M., Varnhagen C., Gold P.E. A memory-enhancing emotionally arousing narrative increases blood glucose levels in human subjects. Psychobiology 1999, 27:386-396.
67. Parkes M., White K.G. Glucose attenuation of memory impairments. Behavioral Neuroscience 2000, 114(2):307-319.
68. Parsons M.W., Gold P.E. Glucose enhancement of memory in elderly humans: An inverted-U dose-response curve. Neurobiology of Aging 1992, 13(3):401-404.
69. Paula F.J., Pimenta W.P., Saad M.J., Paccola G.M., Piccinato C.E., Foss M.C. Sex-related differences in peripheral glucose metabolism in normal subjects. Diabetes & Metabolism 1990, 16(3):234-239.
70. Ragozzino M.E., Gold P.E. Task-dependent effects of intra-amygdala morphine injections: Attenuation by intra-amygdala glucose injections. Journal of Neuroscience 1994, 14(12):7478-7485.
71. Ragozzino M.E., Gold P.E. Glucose injections into the medial septum reverse the effects of intraseptal morphine infusions on hippocampal acetylcholine output and memory. Neuroscience 1995, 68(4):981-988.
72. Ragozzino M.E., Pal S.N., Unick K., Stefani M.R., Gold P.E. Modulation of hippocampal acetylcholine release and spontaneous alternation scores by intrahippocampal glucose injections. The Journal of Neuroscience 1998, 18(4):1595-1601.
73. Ragozzino M.E., Unick K.E., Gold P.E. Hippocampal acetylcholine release during memory testing in rats: Augmentation by glucose. Proceedings of the National Academy of Sciences of the United States of America 1996, 93(10):4693-4698.
74. Ragozzino M.E., Wenk G.L., Gold P.E. Glucose attenuates a morphine-induced decrease in hippocampal acetylcholine output: An in vivo microdialysis study in rats. Brain Research 1994, 655(1-2):77-82.
75. Rahner-Welsch S., Vogel J., Kuschinsky W. Regional congruence and divergence of glucose transporters (GLUT1) and capillaries in rat brains. Journal of Cerebral Blood Flow and Metabolism 1995, 15(4):681-686.
76. Rashidy-Pour A. ATP-sensitive potassium channels mediate the effects of a peripheral injection of glucose on memory storage in an inhibitory avoidance task. Behavioural Brain Research 2001, 126(1-2):43-48.
77. Riby L.M., McLaughlin J., Riby D.M., Graham C. Lifestyle, glucose regulation and the cognitive effects of glucose load in middle-aged adults. British Journal of Nutrition 2008, 100(5):1128-1134.
78. Riby L.M., McMurtrie H., Smallwood J., Ballantyne C., Meikle A., Smith E. The facilitative effects of glucose ingestion on memory retrieval in younger and older adults: Is task difficulty or task domain critical?. British Journal of Nutrition 2006, 95(2):414-420.
79. Riby L.M., Meikle A., Glover C. The effects of age, glucose ingestion and gluco-regulatory control on episodic memory. Age and Ageing 2004, 33(5):483-487.
80. Riby L.M., Sunram-Lea S.I., Graham C., Foster J.K., Cooper T., Moodie C., et al. P3b versus P3a: An event-related potential investigation of the glucose facilitation effect. Journal of Psychopharmacology 2008, 22(5):486-492.
81. Scholey A.B., Harper S., Kennedy D.O. Cognitive demand and blood glucose. Physiology and Behavior 2001, 73(4):585-592.
82. Scholey A.B., Laing S., Kennedy D.O. Blood glucose changes and memory: Effects of manipulating emotion and mental effort. Biological Psychology 2006, 71:12-19.
83. Scholey A.B., Sunram-Lea S.I., Greer J., Elliott J., Kennedy D.O. Glucose administration prior to a divided attention task improves tracking performance but not word recognition: Evidence against differential memory enhancement?. Psychopharmacology 2009, 202(1-3):549-558.
84. Schott B.H., Richardson-Klavehn A., Henson R.N., Becker C., Heinze H.J., Duzel E. Neuroanatomical dissociation of encoding processes related to priming and explicit memory. Journal of Neuroscience 2006, 26(3):792-800.
85. Schroeder J.P., Packard M.G. Systemic or intra-amygdala injections of glucose facilitate memory consolidation for extinction of drug-induced conditioned reward. European Journal of Neuroscience 2003, 17(7):1482-1488.
86. Smith M.A., Riby L.M., Sunram-Lea S.I., van Eekelen J.A., Foster J.K. Glucose modulates event-related potential components of recollection and familiarity in healthy adolescents. Psychopharmacology 2009, 205(1):11-20.
87. Song Z., Levin B.E., McArdle J.J., Bakhos N., Routh V.H. Convergence of pre- and postsynaptic influences on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 2001, 50:2673-2681.
88. Squire L.R., Zola-Morgan S. The medial temporal lobe memory system. Science 1991, 253(5026):1380-1386.
89. Stefani M.R., Gold P.E. Intra-septal injections of glucose and glibenclamide attenuate galanin-induced spontaneous alternation performance deficits in the rat. Brain Research 1998, 813(1):50-56.
90. Stefani M.R., Gold P.E. Intrahippocampal infusions of K-ATP channel modulators influence spontaneous alternation performance: Relationships to acetylcholine release in the hippocampus. Journal of Neuroscience 2001, 21(2):609-614.
91. Stefani M.R., Nicholson G.M., Gold P.E. ATP-sensitive potassium channel blockade enhances spontaneous alternation performance in the rat: A potential mechanism for glucose-mediated memory enhancement. Neuroscience 1999, 93(2):557-563.
92. Stone W.S., Seidman L.J., Wojcik J.D., Green A.I. Glucose effects on cognition in schizophrenia. Schizophrenia Research 2003, 62(1-2):93-103.
93. Stone W.S., Thermenos H.W., Tarbox S.I., Poldrack R.A., Seidman L.J. Medial temporal and prefrontal lobe activation during verbal encoding following glucose ingestion in schizophrenia: A pilot fMRI study. Neurobiology of Learning and Memory 2005, 83(1):54-64.
94. Sunram-Lea S.I., Dewhurst S.A., Foster J.K. The effect of glucose administration on the recollection and familiarity components of recognition memory. Biological Psychology 2008, 77(1):69-75.
95. Sunram-Lea S.I., Foster J.K., Durlach P., Perez C. Investigation into the significance of task difficulty and divided allocation of resources on the glucose memory facilitation effect. Psychopharmacology 2002, 160(4):387-397.
96. Takata K., Hirano H., Kasahara M. Transport of glucose across the blood-tissue barriers. International Reviews in Cytology 1997, 172:1-53.
97. Tulving E. Episodic memory: From mind to brain. Annual Review of Psychology 2002, 53:1-25.
98. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15(1):273-289.
99. Wagner A.D., Koutstaal W., Schacter D.L. When encoding yields remembering: Insights from event-related neuroimaging. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 1999, 354(1387):1307-1324.
100. Wang R., Liu X., Hentges S.T., Dunn-Meynell A.A., Levin B.E., Wang W., et al. The regulation of glucose-excited neurons in the hypothalamic arcuate nucleus by glucose and feeding-relevant peptides. Diabetes 2004, 53:1959-1965.
101. Wenk G.L. An hypothesis on the role of glucose in the mechanism of action of cognitive enhancers. Psychopharmacology 1989, 99(4):431-438.