Serotonin at the level of the amygdala and orbitofrontal cortex modulates distinct aspects of positive emotion in primates

Man, Mei-See; Mikheenko, Yevheniia; Braesicke, Katrin; Cockcroft, Gemma; Roberts, Angela

doi:10.1017/s1461145711000587

Cited by 10 publications

(12 citation statements)

References 73 publications

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“…Anatomical studies in rhesus monkeys and macaques have revealed that innervation of the medial orbitofrontal cortex arises specifically from the DRI region, that is, in the caudal part of the dorsal raphe nucleus, between the medial longitudinal fasciculi (Porrino and Goldman-Rakic, 1982 ; Cavada et al, 2000 ). Together with emerging evidence that serotonin functions in the orbitofrontal cortex to either facilitate exploitation of current resources or exploration of alternatives based on reward expectations (Roberts, 2011 ), and to coordinate positive affective responses (Man et al, 2012 ), these findings are consistent with a potential role of DRI serotonergic neurons projecting to the medial orbitofrontal cortex in positive affective responses to warm temperature. DRI neurons also appear to innervate the ventral striatum (Van Bockstaele et al, 1993 ) and anterior cingulate cortex (Porrino and Goldman-Rakic, 1982 ), regions that, together with the medial orbitofrontal cortex, show correlations with subjective pleasantness ratings made to warm and cold stimuli (Rolls et al, 2008 ).…”

Section: Brain-body Circuitry Linking Non-noxious Thermosensation To supporting

confidence: 64%

Somatic influences on subjective well-being and affective disorders: the convergence of thermosensory and central serotonergic systems

et al. 2015

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Current theories suggest that the brain is the sole source of mental illness. However, affective disorders, and major depressive disorder (MDD) in particular, may be better conceptualized as brain-body disorders that involve peripheral systems as well. This perspective emphasizes the embodied, multifaceted physiology of well-being, and suggests that afferent signals from the body may contribute to cognitive and emotional states. In this review, we focus on evidence from preclinical and clinical studies suggesting that afferent thermosensory signals contribute to well-being and depression. Although thermoregulatory systems have traditionally been conceptualized as serving primarily homeostatic functions, increasing evidence suggests neural pathways responsible for regulating body temperature may be linked more closely with emotional states than previously recognized, an affective warmth hypothesis. Human studies indicate that increasing physical warmth activates brain circuits associated with cognitive and affective functions, promotes interpersonal warmth and prosocial behavior, and has antidepressant effects. Consistent with these effects, preclinical studies in rodents demonstrate that physical warmth activates brain serotonergic neurons implicated in antidepressant-like effects. Together, these studies suggest that (1) thermosensory pathways interact with brain systems that control affective function, (2) these pathways are dysregulated in affective disorders, and (3) activating warm thermosensory pathways promotes a sense of well-being and has therapeutic potential in the treatment of affective disorders.

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Section: Brain-body Circuitry Linking Non-noxious Thermosensation To supporting

confidence: 64%

Somatic influences on subjective well-being and affective disorders: the convergence of thermosensory and central serotonergic systems

et al. 2015

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“…Electrophysiological studies have shown that 5-HT inhibits pyramidal cell firing in the OFC (Rueter et al, 2000;Wallace et al, 2014). The depletion of brain 5-HT or chronic intermittent stress, which reduces frontal cortex 5-HT release, impairs the ability of animals to adapt their response to changes in reward contingencies in the environment, resulting in perseverative behaviour (Bondi et al, 2008;Clarke et al, 2007;Man et al, 2012). Furthermore, increasing serotonergic tone with acute or chronic SSRI treatments has been reported to enhance cognitive flexibility and to decrease perseverative behaviours (Bari et al, 2010;Furr et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

Conditional inactivation of Npy1r gene in mice induces behavioural inflexibility and orbitofrontal cortex hyperactivity that are reversed by escitalopram

et al. 2018

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Cognitive flexibility is the ability to rapidly adapt established patterns of behaviour in the face of changing circumstance and depends critically on the orbitofrontal cortex (OFC). Impaired flexibility also results from altered serotonin transmission in the OFC. The Y1 (Y1R) and Y5 (Y5R) receptors for neuropeptide Y (NPY) colocalize in several brain regions and have overlapping functions in regulating cognition and emotional behaviour. The targeted disruption of gene encoding Y1R (Npy1r gene) in Y5R containing neurons (Npy1r mice) increases anxiety-like behaviour and spatial reference memory. Here we used the same conditional system to analyse whether the coordinated expression of the Y1R and Y5R might be required for behavioural flexibility in reversal learning tasks, OFC serotoninergic tone and OFC neural activity, as detected by immunohistochemical quantification of the immediate-early gene, c-Fos. In addition, we investigated whether the acute treatment of Npy1r mice with the selective serotonin reuptake inhibitor escitalopram affected behavioural flexibility and OFC c-Fos expression. Npy1r male mice exhibit an impairment in performing the reversal task of the Morris water maze and the water T-maze but normal spatial learning, working memory and sociability, compared to their control siblings. Furthermore, Npy1r male mice display decreased 5-hydroxytriptamine (5-HT) positive fibres and increased baseline neural activity in OFC. Importantly, escitalopram normalizes OFC neural activity and restores behavioural flexibility of Npy1r male mice. These findings suggest that the inactivation of Y1R in Y5R containing neurons increases pyramidal neuron activity and dysregulates serotoninergic tone in OFC, whereby contributing to reversal learning impairment.

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“…For example, in a recent study by Man and colleagues (2011), serotonergic lesions of the primate amygdala received late in life failed to disrupt appetitive Pavlovian learning but did retard the ability to generate changes in heart rate. Similar findings were also found in animals of the current study.…”

Section: Discussionmentioning

confidence: 99%

Effects of neonatal amygdala lesions on fear learning, conditioned inhibition, and extinction in adult macaques.

Kazama

Heuer

Davis

et al. 2012

Behavioral Neuroscience

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Fear conditioning studies have demonstrated the critical role played by the amygdala in emotion processing. Although all lesion studies until now investigated the effect of adult-onset damage on fear conditioning, the current study assessed fear-learning abilities, as measured by fear-potentiated startle, in adult monkeys that had received neonatal neurotoxic amygdala damage or sham-operations. After fear acquisition, their abilities to learn and use a safety cue to modulate their fear to the conditioned cue, and, finally, to extinguish their response to the fear conditioned cue were measured with the AX+/BX− Paradigm. Neonatal amygdala damage retarded, but did not completely abolish, the acquisition of a learned fear. After acquisition of the fear signal, four of the six animals with neonatal amygdala lesions discriminated between the fear and safety cues and were also able to use the safety signal to reduce the potentiated-startle response and to extinguish the fear response when the air-blast was absent. In conclusion, the present results support the critical contribution of the amygdala during the early phases of fear conditioning that leads to quick, robust responses to potentially threatening stimuli, a highly adaptive process across all species and likely to be present in early infancy. The neonatal amygdala lesions also indicated the presence of amygdala-independent alternate pathways that are capable to support fear learning in the absence of a functional amygdala. This parallel processing of fear responses within these alternate pathways was also sufficient to support the ability to flexibly modulate the magnitude of the fear responses.

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Serotonin at the level of the amygdala and orbitofrontal cortex modulates distinct aspects of positive emotion in primates

Cited by 10 publications

References 73 publications

Somatic influences on subjective well-being and affective disorders: the convergence of thermosensory and central serotonergic systems

Somatic influences on subjective well-being and affective disorders: the convergence of thermosensory and central serotonergic systems

Conditional inactivation of Npy1r gene in mice induces behavioural inflexibility and orbitofrontal cortex hyperactivity that are reversed by escitalopram

Effects of neonatal amygdala lesions on fear learning, conditioned inhibition, and extinction in adult macaques.

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