Toward Understanding the Neurobiology of Social Attachment: Role of Estrogen Receptors in the Medial Amygdala

Trezza, Viviana; Campolongo, Patrizia

doi:10.1523/jneurosci.5193-08.2009

Cited by 10 publications

(8 citation statements)

References 6 publications

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“…Considering the rewarding effects of chocolate in mice (Hsu et al, 2010, Martin-Garcia et al, 2011), we think that the increase in cataplexy with chocolate is mainly due to increases in positive affect. A final limitation is that we cannot be certain that this reduction was due to a disruption of positive affect because cataplexy was reduced in all three conditions, but a growing literature demonstrates many roles for the amygdala in mediating positive affect (Garavan et al, 2001, Baxter and Murray, 2002, Balleine and Killcross, 2006, Paton et al, 2006, Straube et al, 2008, Trezza and Campolongo, 2009). In narcoleptic dogs and people, cataplexy is clearly triggered by rewarding stimuli and positive emotional states (Gelineau, 1880, Siegel et al, 1989, Overeem et al, 2011), and in narcoleptic mice, cataplexy is increased by stimuli that presumably trigger positive affect (Espana et al, 2007, Clark et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Amygdala Lesions Reduce Cataplexy in Orexin Knock-Out Mice

Burgess

Oishi

Mochizuki

et al. 2013

Journal of Neuroscience

101

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Narcolepsy is characterized by excessive sleepiness and cataplexy, sudden episodes of muscle weakness during waking that are thought to be an intrusion of REM sleep muscle atonia into wakefulness. One of the most striking aspects of cataplexy is that it is often triggered by strong, generally positive emotions, but little is known about the neural pathways through which positive emotions trigger muscle atonia. We hypothesized that the amygdala is functionally important for cataplexy because the amygdala has a role in processing emotional stimuli and it contains neurons that are active during cataplexy. Using anterograde and retrograde tracing in mice, we found that GABAergic neurons in the central nucleus of the amygdala heavily innervate neurons that maintain waking muscle tone such as those in the ventrolateral periaqueductal grey, lateral pontine tegmentum, locus coeruleus, and dorsal raphe. We then found that bilateral, excitotoxic lesions of the amygdala markedly reduced cataplexy in orexin knockout mice, a model of narcolepsy. These lesions did not alter basic sleep/wake behavior, but substantially reduced the triggering of cataplexy. Lesions also reduced the cataplexy events triggered by conditions associated with high arousal and positive emotions (i.e., wheel running and chocolate). These observations demonstrate that the amygdala is a functionally important part of the circuitry underlying cataplexy and suggest that increased amygdala activity in response to emotional stimuli could directly trigger cataplexy by inhibiting brainstem regions that suppress muscle atonia.

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Section: Discussionmentioning

confidence: 99%

Amygdala Lesions Reduce Cataplexy in Orexin Knock-Out Mice

Burgess

Oishi

Mochizuki

et al. 2013

Journal of Neuroscience

101

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“…It also has been suggested that studying the role of ERα in the BST in regulating male social behavior is an essential next step [26]. Therefore the objectives of this study were to test the prediction that increasing ERα in the BST would reduce the expression of male prosocial behavior and to determine if the enhancing ERα in the BST had the same or different effects on male prosocial behavior as it did in the MeA.…”

Section: Introductionmentioning

confidence: 99%

Estrogen Receptor-α in the Bed Nucleus of the Stria Terminalis Regulates Social Affiliation in Male Prairie Voles (Microtus ochrogaster)

et al. 2010

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Estrogen receptor alpha (ERα) typically masculinizes male behavior, while low levels of ERα in the medial amygdala (MeA) and the bed nucleus of the stria terminalis (BST) are associated with high levels of male prosocial behavior. In the males of the highly social prairie vole (Microtus ochrogaster), increasing ERα in the MeA inhibited the expression of spontaneous alloparental behavior and produced a preference for novel females. To test for the effects of increased ERα in the BST, a viral vector was used to enhance ERα expression in the BST of adult male prairie voles. Following treatment, adult males were tested for alloparental behavior with 1–3-day-old pups, and for heterosexual social preference and affiliation. Treatment did not affect alloparental behavior as 73% of ERα-BST males and 62.5% of control males were alloparental. Increasing ERα in the BST affected heterosexual affiliation, with ERα-BST males spending significantly less total time in side-by-side contact with females relative to time spent with control males. ERα-BST males did not show a preference for either the familiar or novel female. These findings differed significantly from those reported in ERα-MeA enhanced males, where ERα inhibited alloparental behavior and produced a preference for a novel female. The findings from this study suggest two things: first, that increased ERα in the BST decreases social affiliation and second, that altering ERα in different regions of the social neural circuit differentially impacts the expression of social behavior.

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“…Results from the large and unpredictable electrolytic lesions used in the rat studies may confound our understanding of amygdaloid organization because they do not take into account its heterogeneous nuclear arrangement and their related functions. For example, γ-aminobutyric acid (GABA) is associated with distinct roles in different subnuclei: aggression and anxiety with central nucleus of the amygdala ( 14 , 15 ), fear extinction with basolateral amygdala ( 16 ), and social behaviors with medial amygdala (MeA) ( 17 ). However, the effect of lesioning specific subnuclei within the amygdala on puberty has not yet been established, and little is known of the potential impact on the pubertal timing of GABAergic or glutamatergic signaling in individual amygdala subnuclei.…”

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confidence: 99%

The Posterodorsal Medial Amygdala Regulates the Timing of Puberty Onset in Female Rats

Hanley

et al. 2015

Endocrinology

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Obesity is the major risk factor for early puberty, but emerging evidence indicates other factors including psychosocial stress. One key brain region notable for its role in controlling calorie intake, stress, and behavior is the amygdala. Early studies involving amygdala lesions that included the medial nucleus advanced puberty in rats. More recently it was shown that a critical site for lesion-induced hyperphagia and obesity is the posterodorsal subnucleus of the medial amygdala (MePD), which may explain the advancement of puberty. Glutamatergic activity also increases in the MePD during puberty without a corresponding γ-aminobutyric acid (GABA)ergic change, suggesting an overall activation of this brain region. In the present study, we report that neurotoxic lesioning of the MePD advances puberty and increases weight gain in female rats fed a normal diet. However, MePD lesioned rats fed a 25% nonnutritive bulk diet also showed the dramatic advancement of puberty but without the increase in body weight. In both dietary groups, MePD lesions resulted in an increase in socialization and a decrease in play fighting behavior. Chronic GABAA receptor antagonism in the MePD from postnatal day 21 for 14 days also advanced puberty, increased socialization, and decreased play fighting without altering body weight, whereas glutamate receptor antagonism delayed puberty and decreased socialization without affecting play fighting. In conclusion, our results suggest the MePD regulates the timing of puberty via a novel mechanism independent of change in body weight and caloric intake. MePD glutamatergic systems advance the timing of puberty whereas local GABAergic activation results in a delay.

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Toward Understanding the Neurobiology of Social Attachment: Role of Estrogen Receptors in the Medial Amygdala

Cited by 10 publications

References 6 publications

Amygdala Lesions Reduce Cataplexy in Orexin Knock-Out Mice

Amygdala Lesions Reduce Cataplexy in Orexin Knock-Out Mice

Estrogen Receptor-α in the Bed Nucleus of the Stria Terminalis Regulates Social Affiliation in Male Prairie Voles (Microtus ochrogaster)

The Posterodorsal Medial Amygdala Regulates the Timing of Puberty Onset in Female Rats

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