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Behavior-associated and post-consumption glucose entry into the nucleus accumbens extracellular space during glucose free-drinking in trained rats.

Wakabayashi KT, Kiyatkin EA - Front Behav Neurosci (2015)

Bottom Line: Glucose is the primary energetic substrate for the metabolic activity of brain cells and its proper delivery from the arterial blood is essential for neural activity and normal brain functions.We found that the drinking behavior is highly cyclic and is associated with relatively large and prolonged increases in extracellular glucose levels.These increases had two distinct components: a highly phasic but relatively small behavior-related rise and a larger tonic elevation that results from the arrival of consumed glucose into the brain's extracellular space.

View Article: PubMed Central - PubMed

Affiliation: In-Vivo Electrophysiology Unit, Behavioral Neuroscience Branch, National Institute on Drug Abuse-Intramural Research Program, National Institutes of Health Baltimore, MD, USA.

ABSTRACT
Glucose is the primary energetic substrate for the metabolic activity of brain cells and its proper delivery from the arterial blood is essential for neural activity and normal brain functions. Glucose is also a unique natural reinforcer, supporting glucose-drinking behavior without food or water deprivation. While it is known that glucose enters brain tissue via gradient-dependent facilitated diffusion, it remains unclear how glucose levels are changed during natural behavior and whether the direct central action of ingested glucose can be involved in regulating glucose-drinking behavior. Here, we used glucose biosensors with high-speed amperometry to examine the pattern of phasic and tonic changes in extracellular glucose in the nucleus accumbens (NAc) during unrestricted glucose-drinking in well-trained rats. We found that the drinking behavior is highly cyclic and is associated with relatively large and prolonged increases in extracellular glucose levels. These increases had two distinct components: a highly phasic but relatively small behavior-related rise and a larger tonic elevation that results from the arrival of consumed glucose into the brain's extracellular space. The large post-ingestion increases in NAc glucose began minutes after the cessation of drinking and were consistently associated with periods of non-drinking, suggesting that the central action of ingested glucose could inhibit drinking behavior by inducing a pause in activity between repeated drinking bouts. Finally, the difference in NAc glucose responses found between active, behavior-mediated and passive glucose delivery via an intra-gastric catheter confirms that motivated behavior is also associated with metabolic glucose use by brain cells.

No MeSH data available.


Related in: MedlinePlus

Changes in NAc [glucose] induced by intra-gastric glucose injections. Panel (A) shows overall changes in NAc glucose for 60 min after intra-gastric glucose injections (4 and 8 ml) and after drinking (mean 5.17 ml) in the same rats (30-s bins). (B) compares the duration and magnitude of the response (as area under the curve) for each condition in (A), where there was an overall main effect (One-Way RM ANOVA, F(2,4) = 9.45, p < 0.05), and the difference between 8 mg and drinking approached significance p = 0.051. (C) compares the initial response between all rats when they began drinking as a result of the tube presentation, and when a subset of rats received an intragastric injection of glucose (4 and 8 mg), relative to the pre-presentation and pre-injection baseline, respectively. During this time interval the response to a 4 and 8 ml intragastric injection was not significantly different, and was combined. For clarity, error bars not shown.
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Figure 4: Changes in NAc [glucose] induced by intra-gastric glucose injections. Panel (A) shows overall changes in NAc glucose for 60 min after intra-gastric glucose injections (4 and 8 ml) and after drinking (mean 5.17 ml) in the same rats (30-s bins). (B) compares the duration and magnitude of the response (as area under the curve) for each condition in (A), where there was an overall main effect (One-Way RM ANOVA, F(2,4) = 9.45, p < 0.05), and the difference between 8 mg and drinking approached significance p = 0.051. (C) compares the initial response between all rats when they began drinking as a result of the tube presentation, and when a subset of rats received an intragastric injection of glucose (4 and 8 mg), relative to the pre-presentation and pre-injection baseline, respectively. During this time interval the response to a 4 and 8 ml intragastric injection was not significantly different, and was combined. For clarity, error bars not shown.

Mentions: Passive administration of glucose via an intra-gastric catheter resulted in a large elevation of NAc glucose levels (Figure 4A). While the latency and the initial components of the response were similar for both doses (Figure 4A, 4 and 8 ml or 400 and 800 mg), the amplitude and duration of the response expressed as the area under the curve was larger for the large-dose injection (Figure 4B; F(2,4) = 9.45, p < 0.05). Importantly, the increase induced by passive glucose injection was qualitatively larger than that occurring after glucose drinking despite a larger volume of consumed glucose. Although the second, slower increase in glucose levels were generally similar within the first 5 min regardless of the dose or route of delivery, we found clear differences in glucose dynamics between tube presentation-mediated consumption and passive glucose delivery within the first 60 s of analysis (Figure 4C). Within this short window, in behaving rats glucose levels phasically increased relative to pre-test baseline before drinking began (i.e., after the tube presentation) and rapidly decreased at the onset of drinking. Comparatively, these changes are noticeably absent in rats receiving a similar volume of glucose intra-gastrically. This relatively small but unique difference may represent the functional contribution of the NAc towards initiating consummatory behavior under stimulus control.


Behavior-associated and post-consumption glucose entry into the nucleus accumbens extracellular space during glucose free-drinking in trained rats.

Wakabayashi KT, Kiyatkin EA - Front Behav Neurosci (2015)

Changes in NAc [glucose] induced by intra-gastric glucose injections. Panel (A) shows overall changes in NAc glucose for 60 min after intra-gastric glucose injections (4 and 8 ml) and after drinking (mean 5.17 ml) in the same rats (30-s bins). (B) compares the duration and magnitude of the response (as area under the curve) for each condition in (A), where there was an overall main effect (One-Way RM ANOVA, F(2,4) = 9.45, p < 0.05), and the difference between 8 mg and drinking approached significance p = 0.051. (C) compares the initial response between all rats when they began drinking as a result of the tube presentation, and when a subset of rats received an intragastric injection of glucose (4 and 8 mg), relative to the pre-presentation and pre-injection baseline, respectively. During this time interval the response to a 4 and 8 ml intragastric injection was not significantly different, and was combined. For clarity, error bars not shown.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4488749&req=5

Figure 4: Changes in NAc [glucose] induced by intra-gastric glucose injections. Panel (A) shows overall changes in NAc glucose for 60 min after intra-gastric glucose injections (4 and 8 ml) and after drinking (mean 5.17 ml) in the same rats (30-s bins). (B) compares the duration and magnitude of the response (as area under the curve) for each condition in (A), where there was an overall main effect (One-Way RM ANOVA, F(2,4) = 9.45, p < 0.05), and the difference between 8 mg and drinking approached significance p = 0.051. (C) compares the initial response between all rats when they began drinking as a result of the tube presentation, and when a subset of rats received an intragastric injection of glucose (4 and 8 mg), relative to the pre-presentation and pre-injection baseline, respectively. During this time interval the response to a 4 and 8 ml intragastric injection was not significantly different, and was combined. For clarity, error bars not shown.
Mentions: Passive administration of glucose via an intra-gastric catheter resulted in a large elevation of NAc glucose levels (Figure 4A). While the latency and the initial components of the response were similar for both doses (Figure 4A, 4 and 8 ml or 400 and 800 mg), the amplitude and duration of the response expressed as the area under the curve was larger for the large-dose injection (Figure 4B; F(2,4) = 9.45, p < 0.05). Importantly, the increase induced by passive glucose injection was qualitatively larger than that occurring after glucose drinking despite a larger volume of consumed glucose. Although the second, slower increase in glucose levels were generally similar within the first 5 min regardless of the dose or route of delivery, we found clear differences in glucose dynamics between tube presentation-mediated consumption and passive glucose delivery within the first 60 s of analysis (Figure 4C). Within this short window, in behaving rats glucose levels phasically increased relative to pre-test baseline before drinking began (i.e., after the tube presentation) and rapidly decreased at the onset of drinking. Comparatively, these changes are noticeably absent in rats receiving a similar volume of glucose intra-gastrically. This relatively small but unique difference may represent the functional contribution of the NAc towards initiating consummatory behavior under stimulus control.

Bottom Line: Glucose is the primary energetic substrate for the metabolic activity of brain cells and its proper delivery from the arterial blood is essential for neural activity and normal brain functions.We found that the drinking behavior is highly cyclic and is associated with relatively large and prolonged increases in extracellular glucose levels.These increases had two distinct components: a highly phasic but relatively small behavior-related rise and a larger tonic elevation that results from the arrival of consumed glucose into the brain's extracellular space.

View Article: PubMed Central - PubMed

Affiliation: In-Vivo Electrophysiology Unit, Behavioral Neuroscience Branch, National Institute on Drug Abuse-Intramural Research Program, National Institutes of Health Baltimore, MD, USA.

ABSTRACT
Glucose is the primary energetic substrate for the metabolic activity of brain cells and its proper delivery from the arterial blood is essential for neural activity and normal brain functions. Glucose is also a unique natural reinforcer, supporting glucose-drinking behavior without food or water deprivation. While it is known that glucose enters brain tissue via gradient-dependent facilitated diffusion, it remains unclear how glucose levels are changed during natural behavior and whether the direct central action of ingested glucose can be involved in regulating glucose-drinking behavior. Here, we used glucose biosensors with high-speed amperometry to examine the pattern of phasic and tonic changes in extracellular glucose in the nucleus accumbens (NAc) during unrestricted glucose-drinking in well-trained rats. We found that the drinking behavior is highly cyclic and is associated with relatively large and prolonged increases in extracellular glucose levels. These increases had two distinct components: a highly phasic but relatively small behavior-related rise and a larger tonic elevation that results from the arrival of consumed glucose into the brain's extracellular space. The large post-ingestion increases in NAc glucose began minutes after the cessation of drinking and were consistently associated with periods of non-drinking, suggesting that the central action of ingested glucose could inhibit drinking behavior by inducing a pause in activity between repeated drinking bouts. Finally, the difference in NAc glucose responses found between active, behavior-mediated and passive glucose delivery via an intra-gastric catheter confirms that motivated behavior is also associated with metabolic glucose use by brain cells.

No MeSH data available.


Related in: MedlinePlus