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Effect of fasting on short-term visual plasticity in adult humans
Silvia Animali1, Cecilia Steinwurzel2,3, Angela Dardano4
1Department of Surgical, Medical and Molecular Pathology and Critical Care Medicine, University of Pisa, Pisa, Italy.
Abstract:
Brain plasticity and function is impaired in conditions of metabolic dysregulation, such as obesity. Less is known on whether brain function is also affected by transient and physiological metabolic changes, such as the alternation between fasting and fed state. Here we asked whether these changes affect the transient shift of ocular dominance that follows short-term monocular deprivation, a form of homeostatic plasticity. We further asked whether variations in three of the main metabolic and hormonal pathways affected in obesity (glucose metabolism, leptin signalling and fatty acid metabolism) correlate with plasticity changes. We measured the effects of 2 h monocular deprivation in three conditions: post-absorptive state (fasting), after ingestion of a standardised meal and during infusion of glucagon-like peptide-1 (GLP-1), an incretin physiologically released upon meal ingestion that plays a key role in glucose metabolism. We found that short-term plasticity was less manifest in fasting than in fed state, whereas GLP-1 infusion did not elicit reliable changes compared to fasting. Although we confirmed a positive association between plasticity and supraphysiological GLP-1 levels, achieved by GLP-1 infusion, we found that none of the parameters linked to glucose metabolism could predict the plasticity reduction in the fasting versus fed state. Instead, this was selectively associated with the increase in plasma beta-hydroxybutyrate (B-OH) levels during fasting, which suggests a link between neural function and energy substrates alternative to glucose. These results reveal a previously unexplored link between homeostatic brain plasticity and the physiological changes associated with the daily fast-fed cycle.
Insights
Brain plasticity, essential for learning, is reduced during fasting. This reduction is linked to increased beta-hydroxybutyrate, suggesting alternative energy sources impact neural function during the fast-fed cycle.
Area of Science:
- Neuroscience
- Metabolic studies
- Physiology
Background:
- Metabolic dysregulation, like obesity, impairs brain plasticity.
- The impact of physiological metabolic shifts, such as fasting and feeding, on brain function remains unclear.
- Homeostatic plasticity, exemplified by ocular dominance shifts after monocular deprivation, is a key indicator of brain adaptability.
Purpose of the Study:
- To investigate how the daily fasting-feeding cycle affects short-term homeostatic brain plasticity.
- To explore the correlation between plasticity changes and key metabolic pathways: glucose metabolism, leptin signaling, and fatty acid metabolism.
- To determine if glucagon-like peptide-1 (GLP-1) influences this form of neural plasticity.
Main Methods:
- Assessed ocular dominance shifts after 2-hour monocular deprivation in three states: fasting, fed, and during GLP-1 infusion.
- Measured metabolic parameters including glucose, leptin, fatty acids, and beta-hydroxybutyrate.
- Correlated plasticity changes with metabolic and hormonal variations.
Main Results:
- Short-term plasticity was significantly reduced in the fasting state compared to the fed state.
- GLP-1 infusion did not reliably alter plasticity compared to fasting, despite a positive association with supraphysiological levels.
- Reduced plasticity during fasting was specifically linked to increased plasma beta-hydroxybutyrate, not glucose metabolism parameters.
Conclusions:
- The daily fasting-feeding cycle dynamically modulates homeostatic brain plasticity.
- Increased beta-hydroxybutyrate during fasting, rather than altered glucose metabolism, is associated with reduced neural plasticity.
- This suggests a role for alternative energy substrates in regulating brain function and plasticity during physiological metabolic shifts.
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