c-Fos protein expression is increased in cholinergic neurons of the rodent basal forebrain during spontaneous and induced wakefulness

Mckenna, James T; Cordeira, Joshua; Jeffrey, Brianne A; Ward, Christopher P.; Winston, Stuart; McCarley, Robert W.; Strecker, Robert E.

doi:10.1016/j.brainresbull.2009.08.015

Cited by 21 publications

(17 citation statements)

References 61 publications

(75 reference statements)

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“…Our observations of Fos expression in the BF of NA grass rats were not in agreement with those reported for nocturnal laboratory rats that were forced to stay awake during their rest phase [13, 14]. We reasoned that this discrepancy could be related to the fact that NA grass rats were voluntarily awake, rather than forced to be awake as it was the case in the experiments with laboratory rats [13, 14]. Further, the elevated expression of Fos seen in reward areas (i.e., SUM and aVTA) in grass rats with access to wheels suggests that enhanced voluntary exercise has rewarding properties, which are not likely shared with situations involving forced wakefulness.…”

Section: Introductioncontrasting

confidence: 96%

“…For example, in lab rats, 2–6 h of induced wakefulness during the resting phase, following procedures similar to the one used in here, elicits high Fos expression in ACh cells of the BF [13, 14, 17]. The discrepancies between our results and the findings in nocturnal rodents could be related to species differences, or are perhaps related to chronotype (i.e., being diurnal vs. being nocturnal).…”

Section: Discussioncontrasting

confidence: 54%

“…Our results also revealed that the effects of forced wakefulness in the brain of grass rats are different from the ones reported for nocturnal rodents [13, 14, 17]. This finding strongly suggests that we must be cautious when generalizing to situations involving humans, the results of experiments with nocturnal animals that are forced to be awake.…”

Section: Discussioncontrasting

confidence: 44%

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Fos expression in arousal and reward areas of the brain in grass rats following induced wakefulness

Castillo‐Ruiz

Núñez

2011

Physiology & Behavior

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In the diurnal grass rat nocturnal voluntary wakefulness induces Fos expression in specific cellular populations of arousal and reward areas of the brain. Here, we evaluated whether involuntary wakefulness would result in similar patterns of Fos expression. We assessed this question using male grass rats that were sleep deprived for 6 h by gentle stimulation (SD group), starting 2 h before lights off (12:12 LD cycle). Then, we examined expression of Fos in cholinergic cells of the basal forebrain (BF), as well as in dopaminergic cells of the reward system, and compared these results to those obtained from an undisturbed control group. Different from previous results with grass rats that were voluntary awake, the BF of SD animals only showed a significant increase in Fos expression in non-cholinergic neurons of the medial septum (MS). These observations differ from reports for nocturnal rodents that are sleep deprived. Thus, our results show that voluntary and induced wakefulness have different effects on neural systems involved in wakefulness and reward, and that the effects of sleep deprivation are different across species. We also investigated whether other arousal promoting regions and circadian and stress related areas responded to sleep deprivation by changing the level of Fos expression. Among these areas, only the lateral hypothalamus (LH) and the ventro lateral preoptic area showed significant effects of sleep deprivation that dissipated after a 2 h period of sleep recovery, as it was also the case for the non-cholinergic MS. In addition, we found that Fos expression in the LH was robustly associated with Fos expression in other arousal and reward areas of the brain. This is consistent with the view that the arousal system of the LH modulates neural activity of other arousal regions of the brain, as described for nocturnal rodents.

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Section: Introductioncontrasting

confidence: 96%

Section: Discussioncontrasting

confidence: 54%

Section: Discussioncontrasting

confidence: 44%

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Fos expression in arousal and reward areas of the brain in grass rats following induced wakefulness

Castillo‐Ruiz

Núñez

2011

Physiology & Behavior

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“…It is known that a majority of BF neurons show tonically increased firing during wakefulness, functionally related to maintenance of cortical arousal and associated cognitive operations (Baxter and Chiba, 1999; Szymusiak et al, 2000; Jones, 2005; Lee et al, 2005). During SD, BF neuronal activity is increased even more than in spontaneous wakefulness, as shown by the degree of Fos immunoreactivity (Greco et al, 2000; Modirrousta et al, 2004; McKenna et al, 2009). A positive correlation between the number of iNOS + /Fos + cells in BF and homeostatic sleep pressure (Fig.…”

Section: Discussionmentioning

confidence: 99%

Sleep Deprivation Triggers Inducible Nitric Oxide-Dependent Nitric Oxide Production in Wake–Active Basal Forebrain Neurons

Kalinchuk¹,

McCarley²,

Porkka‐Heiskanen³

et al. 2010

J. Neurosci.

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Sleep loss negatively impacts performance, mood, memory, and immune function, but the homeostatic factors that impel sleep after sleep loss are imperfectly understood. Pharmacological studies had implicated the basal forebrain (BF) inducible nitric oxide (NO) synthase (iNOS)-dependent NO as a key homeostatic factor, but its cellular source was obscure. To obtain direct evidence about the cellular source of iNOS-generated NO during sleep deprivation (SD), we used intracerebroventricular perfusion in rats of the cell membrane-permeable dye diaminofluorescein-2/diacetate (DAF-2/DA) that, once intracellular, bound NO and fluoresced. To circumvent the effects of neuronal NOS (nNOS), DAF-2/DA was perfused in the presence of an nNOS inhibitor. SD led to DAF-positive fluorescence only in the BF neurons, not glia. SD increased expression of iNOS, which colocalized with NO in neurons and, more specifically, in prolonged wakefulness-active neurons labeled by Fos. SD-induced iNOS expression in wakefulness-active neurons positively correlated with sleep pressure, as measured by the number of attempts to enter sleep. Importantly, SD did not induce Fos or iNOS in stress-responsive central amygdala and paraventricular hypothalamic neurons, nor did SD elevate corticosterone, suggesting that the SD protocol did not provoke iNOS expression through stress. We conclude that iNOS-produced neuronal NO is an important homeostatic factor promoting recovery sleep after SD.

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“…Neuronal activation is indicated by induction of c-Fos (Thakkar et al, 2010; Shiromani et al, 1992; Morgan and Curran, 1991; McKenna et al, 2009). Thus, activation of NAc was examined by monitoring c-Fos expression with immunohistochemistry (IH).…”

Section: Methodsmentioning

confidence: 99%

Nicotine Infusion in the Wake‐Promoting Basal Forebrain Enhances Alcohol‐Induced Activation of Nucleus Accumbens

Sharma

DuMontier

deRoode

et al. 2014

Alcoholism Clin & Exp Res

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Background Nicotine and alcohol co-abuse is highly prevalent. Recently, we have shown that nicotine infusion in the basal forebrain (BF) increases alcohol consumption. Since nucleus accumbens (NAc) is the terminal brain region associated with drug addiction, we hypothesize that nicotine infusion in the BF may enhance alcohol induced activation of NAc. Methods Adult male Sprague-Dawley rats were surgically implanted with bilateral guide cannulas in the BF. Following post-operative recovery, rats were divided into four groups: 1) ACSF+W group received artificial cerebrospinal fluid (ACSF; 500 nl/side) in the BF and systemic water [intragastric (ig); 10 ml/kg; N=5], 2) EtOH group received ACSF in the BF (500 nL/side) and systemic alcohol (ig; 3 g/Kg; N=5), 3) NiC group received nicotine in the BF (75 pmole/500nl/side) and systemic water (ig; 10 mL/Kg; N=5) and 4) NiC+EtOH group received nicotine in the BF (75 pmole/500nl/side) and systemic alcohol (ig; 3 g/Kg; N=5). Rats were euthanized two hours after treatment to examine c-Fos expression in the NAc by immunohistochemistry. Results All injections sites were localized in the BF. Two way ANOVA (ig vs infusion) revealed significant main effects of both treatments (ig and infusion, p < 0.001) on c-Fos expression in the NAc shell but not in the core. Subsequent post-hoc test (Bonferroni’s) revealed that as compared to ACSF+W group, c-Fos expression was significantly increased in the shell of NAc of rats in all three (EtOH, NiC and NiC+EtOH) groups with maximal increase observed in NiC+EtOH group. Conclusions The results suggests: 1) BF nicotine infusion induced c-Fos in both core and the shell region of NAc at levels comparable to those observed after systemic alcohol administration; 2) BF nicotine infusion with systemic alcohol induced a significant additive increase in c-Fos expression only in the NAc shell region. These findings implicate the BF in alcohol and nicotine co-use.

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c-Fos protein expression is increased in cholinergic neurons of the rodent basal forebrain during spontaneous and induced wakefulness

Cited by 21 publications

References 61 publications

Fos expression in arousal and reward areas of the brain in grass rats following induced wakefulness

Fos expression in arousal and reward areas of the brain in grass rats following induced wakefulness

Sleep Deprivation Triggers Inducible Nitric Oxide-Dependent Nitric Oxide Production in Wake–Active Basal Forebrain Neurons

Nicotine Infusion in the Wake‐Promoting Basal Forebrain Enhances Alcohol‐Induced Activation of Nucleus Accumbens

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