Adaptations of Striatal Endocannabinoid System During Stress

Rossi, Silvia; Chiara, Valentina De; Musella, Alessandra; Mataluni, Giorgia; Sacchetti, Lucia; Bernardi, Giorgio; Usiello, Alessandro; Centonze, Diego

doi:10.1007/s12035-009-8061-4

Cited by 7 publications

(5 citation statements)

References 79 publications

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“…Ventral striatum activation was seen during alcohol-cue exposure, while the right dorsal striatum increased during stress exposure. Increases in dorsal striatal activity during stress have been reported previously (Sinha and Li 2007) and chronic stress is known to alter dorsal striatal projections to the frontal cortex (Rossi, et al 2009), supporting the notion that stress influences habit-based decision making involving fronto-striatal pathways (Dias-Ferreira, et al 2009). The ventral striatum (VS) has been associated with reward processing (Haber and Knutson 2010), and our findings of specific activation in the ventral striatum during alcohol context cue exposure is consistent with this observation and previous studies showing VS activation with an alcohol taste cue (Filbey, et al 2008) and intravenous injection of alcohol (Gilman, et al 2008).…”

Section: Discussionsupporting

confidence: 64%

Sex differences in neural responses to stress and alcohol context cues

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Jia

Lacadie

et al. 2010

Human Brain Mapping

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Stress and alcohol context cues are each associated with alcohol-related behaviors, yet neural responses underlying these processes remain unclear. The present study investigated the neural correlates of stress and alcohol context cue experiences and examined sex differences in these responses. Using functional magnetic resonance imaging, brain responses were examined while 43 right-handed, socially drinking, healthy individuals (23 females) engaged in brief guided imagery of personalized stress, alcohol-cue and neutral-relaxing scenarios. Stress and alcohol-cue exposure increased activity in the cortico-limbic-striatal circuit (p<.01, corrected), encompassing the medial prefrontal cortex (mPFC), orbitofrontal cortex (OFC), anterior cingulate cortex (ACC), left anterior insula, striatum and visuomotor regions (parietal and occipital lobe, and cerebellum). Activity in the right dorsal striatum increased during stress, while bilateral ventral striatum activity was evident during alcohol-cue exposure. Men displayed greater stress-related activations in the mPFC, rostral ACC, posterior insula, amygdala and hippocampus than women, whereas women showed greater alcohol-cue related activity in the superior and middle frontal gyrus (SFG/MFG) than men. Stress-induced anxiety was positively associated with activity in emotion modulation regions, including the medial OFC, ventromedial PFC, left superior-medial PFC and rostral ACC in men, but in women with activation in the SFG/MFG, regions involved in cognitive processing. Alcohol craving was significantly associated with the striatum (encompassing dorsal and ventral) in men, supporting its involvement in alcohol ‘urge’ in healthy men. These results indicate sex differences in neural processing of stress and alcohol-cue experiences, and have implications for sex-specific vulnerabilities to stress- and alcohol-related psychiatric disorders.

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Section: Discussionsupporting

confidence: 64%

Sex differences in neural responses to stress and alcohol context cues

Seo

Jia

Lacadie

et al. 2010

Human Brain Mapping

168

150

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“…However, chronic handling alone is not sufficient to reverse the abundance of social deprivation-induced changes in cannabinoid receptor densities or endocannabinoid levels. These observations support a pivotal role for the endocannabinoid signaling system in the adaptation to stressful life events (for review see Finn, 2009, Rossi et al, 2009) as well as in emotionality-related disturbances (Leweke and Koethe, 2008, Lutz, 2009). …”

Section: Resultssupporting

confidence: 55%

Social isolation and chronic handling alter endocannabinoid signaling and behavioral reactivity to context in adult rats

et al. 2010

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Social deprivation in early life disrupts emotionality and attentional processes in humans. Rearing rats in isolation reproduces some of these abnormalities, which are attenuated by daily handling. However, the neurochemical mechanisms underlying these responses remain poorly understood. We hypothesized that post-weaning social isolation alters the endocannabinoid system, a neuromodulatory system that controls emotional responding. We characterized behavioral consequences of social isolation and evaluated whether handling would reverse social isolation-induced alterations in behavioral reactivity to context and the endocannabinoid system. At weaning, pups were single or group housed and concomitantly handled or not handled daily until adulthood. Rats were tested in emotionality- and attentional-sensitive behavioral assays (open field, elevated plus maze, startle and prepulse inhibition). Cannabinoid receptor densities and endocannabinoid levels were quantified in a separate group of rats. Social isolation negatively altered behavioral responding. Socially-isolated rats that were handled showed less deficits in the open field, elevated plus maze, and prepulse inhibition tests. Social isolation produced site-specific alterations (supraoptic nucleus, ventrolateral thalamus, rostral striatum) in cannabinoid receptor densities compared to group rearing. Handling altered the endocannabinoid system in neural circuitry controlling emotional expression. Handling altered endocannabinoid content (prefrontal and piriform cortices, nucleus accumbens) and cannabinoid receptor densities (lateral globus pallidus, cingulate and piriform cortices, hippocampus) in a region-specific manner. Some effects of social isolation on the endocannabinoid system were moderated by handling. Isolates were unresponsive to handling-induced increases in cannabinoid receptor densities (caudal striatum, anterior thalamus), but were sensitive to handling-induced increases in endocannabinoid content (piriform cortex), compared to group-reared rats. Our findings suggest alterations in the endocannabinoid system may contribute to the abnormal isolate phenotype. Handling modifies the endocannabinoid system and behavioral reactivity to context, but surmounts only some effects of social isolation. These data implicate a pivotal role for the endocannabinoid system in stress adaptation and emotionality-related disturbances.

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“…We performed electrophysiological measurements of striatal CB1R sensitivity in these mice 1 week after the behavioral tests in order to recover the effect of the stress induced by behavioral manipulation on endocannabinoid system [48]. Of note, the loss of CB1R sensitivity on GABA synapses is a synaptic dysfunction that occurs throughout the disease progression ([46]; present paper]) and IL-1ra treatment was previously shown to ameliorate both the depressive-like behavior of EAE mice in the acute phase of the disease and the dopaminergic dysfunction affecting the striatum [10].…”

Section: Resultsmentioning

confidence: 99%

Interaction between interleukin-1β and type-1 cannabinoid receptor is involved in anxiety-like behavior in experimental autoimmune encephalomyelitis

Gentile

Fresegna

Musella

et al. 2016

J Neuroinflammation

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BackgroundMood disorders, including anxiety and depression, are frequently diagnosed in multiple sclerosis (MS) patients, even independently of the disabling symptoms associated with the disease. Anatomical, biochemical, and pharmacological evidence indicates that type-1 cannabinoid receptor (CB1R) is implicated in the control of emotional behavior and is modulated during inflammatory neurodegenerative diseases such as MS and experimental autoimmune encephalomyelitis (EAE).MethodsWe investigated whether CB1R could exert a role in anxiety-like behavior in mice with EAE. We performed behavioral, pharmacological, and electrophysiological experiments to explore the link between central inflammation, mood, and CB1R function in EAE.ResultsWe observed that EAE-induced anxiety was associated with the downregulation of CB1R-mediated control of striatal GABA synaptic transmission and was exacerbated in mice lacking CB1R (CB1R-KO mice). Central blockade of interleukin-1β (IL-1β) reversed the anxiety-like phenotype of EAE mice, an effect associated with the concomitant rescue of dopamine (DA)-regulated spontaneous behavior, and DA-CB1R neurotransmission, leading to the rescue of striatal CB1R sensitivity.ConclusionsOverall, results of the present investigation indicate that synaptic dysfunction linked to CB1R is involved in EAE-related anxiety and motivation-based behavior and contribute to clarify the complex neurobiological mechanisms underlying mood disorders associated to MS.

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Adaptations of Striatal Endocannabinoid System During Stress

Cited by 7 publications

References 79 publications

Sex differences in neural responses to stress and alcohol context cues

Sex differences in neural responses to stress and alcohol context cues

Social isolation and chronic handling alter endocannabinoid signaling and behavioral reactivity to context in adult rats

Interaction between interleukin-1β and type-1 cannabinoid receptor is involved in anxiety-like behavior in experimental autoimmune encephalomyelitis

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