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Modest decrements in plasma glucose concentration cause early impairment in cognitive function and later activation of glucose counterregulation in the absence of hypoglycemic symptoms in normal man.
Open accessAbstract
To establish the glycemic threshold for onset of neuroglycopenia (impaired cognitive function, measured by the latency of the P300 wave), activation of hormonal counterregulation and hypoglycemic symptoms, 12 normal subjects were studied either under conditions of insulin-induced, glucose-controlled plasma glucose decrements, or during maintenance of euglycemia. A decrement in plasma glucose concentration from 88 +/- 3 to 80 +/- 1 mg/dl for 150 min did not result in changes in the latency of the P300 wave nor in an activation of counterregulatory hormonal response. In contrast, a greater decrement in plasma glucose concentration from 87 +/- 3 to 72 +/- 1 mg/dl for 120 min caused an increase in the latency of the P300 wave (from 301 +/- 12 to 348 +/- 20 ms, P less than 0.01), a subsequent increase in all counterregulatory hormones but no hypoglycemic symptoms. Finally, when plasma glucose concentration was decreased in a stepwise manner from 88 +/- 2 to 50 +/- 1 mg/dl within 75 min, the increase in the latency of the P300 wave was correlated with the corresponding plasma glucose concentration (r = -0.76, P less than 0.001). The glycemic threshold for hypoglycemic symptoms was 49 +/- 2 mg/dl. Thus, in normal man the glycemic threshold for neuroglycopenia (72 +/- 1 mg/dl) is greater than currently thought; the hormonal counterregulation follows the onset of neuroglycopenia; the hypoglycemic symptoms are a late indicator of advanced neuroglycopenia.
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“the patients referred both adrenergic and neuroglyco- penic symptoms at 45 min when plasma glucose concentration was 49±2 mg/dl.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“When plasma glucose concentra- tion was normalized at 105 min, the latency of P300 wave was still greater than in the control study (339±15 vs. 298± 10 ms, P < 0.05).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“The score peak of both adrenergic and neu- roglycopenic symptoms occurred at 75 min at the end of the plateau plasma glucose concentration of 50 mg/dl.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“Only after 30 additional min of euglycemia the latency of P300 wave was normalized (317±13 ms) as com- pared both to baseline values (296±9 ms) and to the control study (309±12 ms) (P = NS).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“Following normalization of plasma glucose, the hypoglycemia symptoms were no longer different from those of the control study (neur- oglycopenic symptoms at 90 min; adrenergic symptoms at 105 min).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“Plasma glucagon increased from 116±10 to 153±16 pg/ml at 90 min (P < 0.05) and remained increased at 162±10 pg/ml throughout the study.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Results
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“the glucose infusion rates decreased between 90 and 180 min from 0.9±0.3mg/kg min to 0.3±0.1 mg/kg.min (P < 0.05).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Results
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“Plasma growth hormone increased from 1.1±0.4 to 4.9±1.5 ng/ml (P < 0.05) at 105 min and continued to increase to a peak value of 10.5±3 ng/ml at 180 min.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Results
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“Plasma cortisol was greater than in the control study from 150 to 180 min ( 17±2 ,ug/dl vs. 10±2 ,ug/dl, P < 0.05) (Fig. 2).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Results
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“In the present studies the latency of the P300 wave evoked by acoustic stimuli was found to be highly reproducible in the same subjects tested several times in euglycemic conditions.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“In contrast, a greater decrement in plasma glucose concentration from 87±3 to 72±1 mg/dl for 120 min caused an increase in the latency of the P300 wave (from 301±12 to 348±20 ms, P < 0.01), a subsequent increase in all counterregulatory hormones but no hypoglycemic symptoms.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Abstract
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“Plasma growth hormone increased significantly at 45 min (13±3.5 vs. 0.7±0.2ng/ml, P < 0.05), peaked at 75 min (26±5.3pg/ml) and remained increased until 90 min (20±3.9ng/ml vs. 2.2±0.5 pg/ml of the control study, P < 0.05).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“in the study in which plasma glucose concentration was allowed to decrease, plasma FFA and B-OH-B concentration increased at 135 min approximately by 100 and 65%, respectively, as compared to baseline.In contrast, in the control study FFA and B-OH-B concentration just approached the baseline values.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“in the study in which plasma glucose concentration was allowed to decrease at 72±1 mg/dl, plasma FFA and B-OH-B initially decreased to nadir values of 0.3±0.05mM at 75 min and 0.126±0.011mM at 90 min, respectively, but subsequently increased despite hyperinsulin- emia to values no longer different from baseline (FFA at 120 min, B-OH-B at 150 min)”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Results
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“A decrement in plasma glucose concentration from 88±3 to 80±1 mg/dl for 150 min did not result in changes in the latency of the P300 wave nor in an activation of counterregulatory hormonal response.”
- Also stated in: § Results · plain
“The latency of the P300 wave and the plasma counterregu- latory hormone concentration did not change either in the control study (euglycemia) or when plasma glucose concen- tration was allowed to decrease from 88±3 to 80±1 mg/dl (Fig. 1).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Abstract
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“Both plasma glucagon and epinephrine increased at 35 min (glucagon from 89±9 to 147±15 pg/ml, epinephrine from 42±12 to 157±29 pg/ml, both P < 0.05), both peaked at 75 min (215±18 and 389±46 pg/ml, respectively) and both remained increased until 90 min (P < 0.05).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“In the present study in which a more sensitive approach to evaluate brain function was used the activation of hormonal counterre- gulation followed rather than preceded the onset of neurogly- copenia, although the absolute glycemic threshold for onset of neuroglycopenia and activation of counterregulation is vir- tually identical.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“When in the present studies the glycemic threshold for hormonal counterregulation was evaluated in the step-wise plasma glucose dec- rement protocol (study B) in which a given plateau plasma glucose concentration was maintained for several minutes, plasma glucagon and epinephrine increased at plasma glucose concentration of -60 mg/dl, and growth hormone and corti- sol at -50 mg/dl.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“However, when the glycemic threshold for activation ofhormonal counterregulation was evaluated in the protocol of single-step decrease in plasma glucose, which was held for at least 120 min (study A), the glycemic threshold was found to be greater (-72 mg/dl) and, most important, it was identical for all counterregulatory hormones.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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“The generation of the P300 wave implies both perception and cognition of task relevant stimuli (acoustic, somatosensorial and visual) and its latency expresses the time required for the complete evaluation of the stimulus (28).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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- Not checked yetcites [28]
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“In our laboratory, the coefficient of variation (c.v.) of the determination of latency of P300 wave determined in 30 normal volunteers (17 male, 13 female; 28±0.3 yr) studied in the fasting state between 9 and 10 a.m. on three different occasions at 2-5-d intervals was 7.2±0.6%.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Methods
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“several studies in man have shown that brain function be- comes impaired when plasma glucose concentration decreases -30-50 mg/dl below normal fasting values, as demonstrated by the abnormalities of neuropsychological tests (3-5), visual reaction time (6), and electroencephalogram (7,8).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Introduction
What the sources say
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“Three sets of experiments were performed in a single blind in six subjects (three male, three female) on three different occasions in random order, a week apart.”
- Also stated in: § Methods · plain
“In all the studies the subjects were unaware of the plasma glucose concentration and were asked to score at 15-min intervals from 0 (none) to 5 (severe) the following symptoms:”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Methods
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“Thus, in normal man the glycemic threshold for neurogly- copenia (72±1 mg/dl) is greater than currently thought;”
- Also stated in: § Study B · hedged
“Thus, it appears that the glycemic threshold for the onset of neuroglycopenia is greater than cur- rently appreciated (3-8, 25, 26)”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Abstract
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- The authors state this as an assumption: Impairment in cognitive function as measured by P300 latency closely reflects impaired brain glucose metabolism (neuroglycopenia).
- Also stated in: § Study B · hedged
In the paper
“plasma lactate concentration does not change in an early phase of hypoglycemia, but increases only in the re- covery phase (37).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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- Not checked yetcites [37]
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In the paper
“More profound decrements in plasma glucose (-35 mg/dl below the postabsorptive values) further impair brain function, exag- gerate hormonal counterregulation and finally result in symp- toms of hypoglycemia.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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- The authors state this as an assumption: Impairment in cognitive function as measured by P300 latency closely reflects impaired brain glucose metabolism (neuroglycopenia).
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In the paper
“since aging (33), dementia (20), Huntington's disease (34) and organic cognitive disorders in children (21) are associated with an increased latency in P300 wave”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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- Not checked yetcites [33]
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In the paper
“although the abso- lute glycemic threshold for onset of neuroglycopenia and acti- vation ofhormonal counterregulation is virtually identical, the onset of the latter follows that of the former.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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- The authors state this as an assumption: Impairment in cognitive function as measured by P300 latency closely reflects impaired brain glucose metabolism (neuroglycopenia).
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In the paper
“Thus, glucose is the obligate fuel for the brain, and more than 90 percent ofthe energy needed for brain function derives from oxidation of glucose (2).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Introduction
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“Since the brain virtually cannot store or synthetize glucose, a constant supply of glucose from the circulation to the central nervous system is essential for normal brain function and whole body survival (1).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Introduction
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In the paper
“it is concluded that the latency of the P300 wave not only is related to some of the most important brain cortical functions in man, but also that such a parameter might be used as a measure of physiological integrity of cognitive function.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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- Not checked yetcites [19]
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In the paper
“Thus, the assumption that the latency of P300 wave is a specific and sensitive measure of cortical cognitive function, which is in turn influenced by brain metabolism, is validated.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
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In the paper
“The statistical significance was evaluated using the analysis of variance corrected for repeated measures (22).The dependent variables were compared dur- ing the hypoglycemic and euglycemic clamps to allow variability in the measurements with time under euglycemic conditions to be factored into the results.”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Methods
What the sources say
- Not checked yetcites [22]
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In the paper
“The P300 wave is the most prominent component of event-related potentials (19,20) and reflects the active cogni- tive processing of the stimulus information by the subject (27).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
What the sources say
- Not checked yetcites [19]
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Probably not a substantial claim. It may state two separate claims as one.
In the paper
“Previous studies in rats have shown that only for a 50% decrease in plasma glucose concentration, the glucose substrate availability becomes the rate limiting step for glycolysis in the brain (2).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
What the sources say
- Not checked yetcites [2]
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim.
In the paper
“Thus, the ob- servation that significant neuroglycopenia developed and hor- monal counterregulation was activated in the absence of symptoms of hypoglycemia, reinforce the concept that the “hypoglycemic symptoms” are a late indicator of plasma glu- cose decrements below normal values, as recently reported by Schwartz et al. (26).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
What the sources say
- Not checked yetcites [26]
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“At present, hypoglycemia is defined as a plasma glucose concentration at which symptoms and signs of brain dysfunc- tion appear, i.e., 55-50 mg/dl (3-7).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
What the sources say
- Not checked yetcites [3]
- Not checked yetcites [4]
- Not checked yetcites [5]
- Not checked yetcites [6]
- Not checked yetcites [7]
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim.
None of the sources cited for this claim have been checked yet.
In the paper
“Actually, it has been shown that the glycemic threshold for activation of counterregulation and symptoms of hypoglycemia is increased in diabetic subjects chronically hyperglycemic (42), whereas it is decreased in diabetics treated with regimens of intensive insulin therapy (42-47) which result in chronically subnormal plasma glucose concentrations (48).”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
What the sources say
- Not checked yetcites [42]
- Not checked yetcites [43]
- Not checked yetcites [44]
- Not checked yetcites [45]
- Not checked yetcites [46]
- Not checked yetcites [47]
- Not checked yetcites [48]
boosteddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
The authors state this as an assumption.
Impairment in cognitive function as measured by P300 latency closely reflects impaired brain glucose metabolism (neuroglycopenia).
“The major finding of the present study, i.e., the exquisite sensitivity of the brain to minor decreases in ambient plasma glucose, relies entirely on the assumption that impairment in cognitive function as measured by means of the latency of the P300 wave, closely reflects impaired brain glucose metabo- lism, i.e., neuroglycopenia.”
The paper relies on this without support.
The potentially deleterious effects of modest plasma glucose decrements on brain function had not been carefully examined before this study.
“However, because the potentially deleterious effects of modest decrements in plasma glucose concentration on brain function have never been carefully examined, it cannot be excluded that the glycemnic threshold for the onset of neuroglycopenia and brain dysfunction is actually greater than what is currently appreciated.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“In addition, it is controversial as to whether the glycaemic threshold for appearance of autonomic symptoms is lower than that of neuroglycopenic symptoms (i.e. a smaller decrease in plasma glucose concentration is sufficient to elicit the autonomic as compared to neuroglycopenic symptoms) [2,3,6].”
In the citing paper
“However, such a discrepancy may be more apparent than real, because the response of cortisol is delayed due to the activation of the adrenal cortex by ACTH, a fact which may lead to an overestimation of the threshold if the glycaemic plateau is not sufficiently prolonged [2,26].”
In the citing paper
“However, our results are in agreement with the majority of previous studies [1,2], including those of Vea et al. [6].”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
“peaked at 75 min (26±5.3pg/ml)”
§ Modest Decrements in Plasma Glucose Concentration Cause Early Impairment in Cognitive Function and Later Activation of Glucose Counterregulation in the Absence of Hypoglycemic Symptoms in Normal Man > Study B
“remained increased until 90 min (20±3.9ng/ml vs. 2.2±0.5 pg/ml of the control study, P < 0.05).”
Citations
Cites
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Coated Charcoal Immunoassay of Insulin
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A simple fluorimetric method for the estimation of free 11-hydroxycorticoids in human plasma
Mattingly, D. (1962) · Journal of Clinical Pathology · doi:10.1136/jcp.15.4.374 · Cited by 1,181
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Endogenous Potentials Generated in the Human Hippocampal Formation and Amygdala by Infrequent Events
Halgren, E., Squires, N. K., Wilson, C. L., Rohrbaugh, J., Babb, T. L., & Crandall, P. H. (1980) · Science · doi:10.1126/science.7434000 · Cited by 778
Research works printed but not linked: 5
- Tamburrano, G., A. Lala, F. Leonetti, N. Locuratolo, and S. Busco. 1987. Electroencefalography during prolonged hypoglycemia. In Hypoglycemia. D. Andreani, V. Marks, and P. J. Lefebvre, editors. Raven Press, New York. 181-194.
- Faloona, G., and R. H. Unger. 1974. Glucagon. In Methods of Hormone Radioimmunoassay. B. Jaffe and H. Behrman, editors. Aca- demic Press, Inc., New York. 317-330.
- Peake, G. 1972. Growth Hormone. In Methods of Hormone Radioimmunoassay. B. Jaffe and H. Berhman, editors. Academic Press, Inc., New York. 103-121.
- Marks, V. and F. C. Rose. 1981. Hypoglycaemia. Blackwell Scientific Publications, Oxford. 1-521.
- Bachelard, H. 1981. Cerebral metabolism and hypoglycaemia. In Hypoglycaemia. V. Marks and F. C. Rose, editors. Blackwell Scien- tific Publications, Oxford. 51-68.
Cited by
Sorted by citations
Mitrakou, A., Ryan, C., Veneman, T., Mokan, M., Jenssen, T., Kiss, I., Durrant, J., Cryer, P., & Gerich, J. (1991) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1991.260.1.e67 · Cited by 558
Glucose administration, heart rate and cognitive performance: effects of increasing mental effort
Kennedy, D. O., & Scholey, A. B. (2000) · Psychopharmacology · doi:10.1007/s002139900335 · Cited by 267
“Transient cognitive impairment has been demonstrated as a result of both hypoglycaemia (Holmes et al. 1984; Gold et al. 1985) and lowered but supra-hypoglycaemic glucose levels (De Feo et al. 1988; Taylor and Rachman 1988).”
BackgroundCarbohydrates and physical/mental performance during intermittent exercise to fatigue
WELSH, R. S., Davis, J. M., BURKE, J. R., & Williams, H. G. (2002) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200204000-00025 · Cited by 222
“In addition, modest changes in glucose within normal ranges can affect cognitive function (9).”
BackgroundFanelli, C., Pampanelli, S., Epifano, L., Rambotti, A. M., Di Vincenzo, A., Modarelli, F., Ciofetta, M., Lepore, M., Annibale, B., Torlone, E., et al. (1994) · Diabetologia · doi:10.1007/bf00399801 · Cited by 212
“Thus, minimal neuroglycopenia after recurrent hypoglycaemia reduces the hormone and symptom responses which would otherwise occur at precise glycaemic thresholds [27, 28, 30, 36, 37 ].”
BackgroundSelf-citationFanelli, C., Pampanelli, S., Epifano, L., Rambotti, A. M., Ciofetta, M., Modarelli, F., Di Vincenzo, A., Annibale, B., Lepore, M., Lalli, C., et al. (1994) · Diabetologia · doi:10.1007/bf00404337 · Cited by 193
“In accordance with previous classifications [1-3, 19], the first five symptoms were considered neuroglycopenic and the last six, autonomic.”
BackgroundResultInfluentialSelf-citation
Metadata
- Authors
- De Feo, P., Gallai, V, Mazzotta, G., Crispino, G., Torlone, E., Perriello, G., Ventura, M. M., Santeusanio, F., Brunetti, P., & Bolli, G. B.
- Affiliations
- University of Perugia (IT)
- Venue
- Journal of Clinical Investigation
- Published
- 1988-08-01
- Volume
- 82
- Issue
- 2
- Pages
- 436-444
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC303532
- OpenAlex
- W2074411447
- Semantic Scholar
- c941f18c807aae8c70851c0868512fdb413432d8
- Cited by
- 138
- References
- 45
- Citations by year
- 2026: 1 · 2023: 2 · 2022: 2 · 2021: 1 · 2019: 1 · 2018: 1 · 2017: 2 · 2016: 1 · 2015: 3 · 2014: 4 · 2013: 4 · 2012: 3
- FWCI
- 3.42
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Consiglio Nazionale delle Ricerche
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
- Health Sciences › Medicine › Clinical Neurology › Neurological and metabolic disorders
- Keywords
- neuroglycopenia, hypoglycemia, plasma glucose, P300 latency, cognitive impairment, glucose counterregulation, counterregulatory hormones, hypoglycemic symptoms, glycemic thresholds, insulin-induced hypoglycemia, normoglycemia
- MeSH terms
- Adult, Blood Glucose, Brain, Cognition Disorders, Fatty Acids, Nonesterified, Female, Glucose, Humans, Hydroxybutyrates, Hypoglycemia, Male, Reaction Time, 3-Hydroxybutyric Acid
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
A language model drew the claims from the paper on 2026-10-04, under version 3 of the claim definition (model deepseek-v4.1-flash, prompt extract-v3).
A second model labelled each claim on 2026-10-04 (model jev-1.13-20260917, definition revision gold-guideline-v0.2).
Statistics and arithmetic are recomputed, not judged.
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