Sex differences in aversive memory in rats: Possible role of extinction and reactive emotional factors

Ribeiro, Alessandra Mussi; Barbosa, Flávio Freitas; Godinho, Monique; Fernandes, Valéria S.; Munguba, Hermany; Melo, Thieza G.; Barbosa, Marla T.; Eufrásio, R; Cabral, Alícia; Izídio, Geison S.; Silva, Regina H.

doi:10.1016/j.bandc.2010.07.012

Cited by 49 publications

(23 citation statements)

References 42 publications

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“…These results are in accordance with previous literature indicating that female rats do not show conditioned freezing in response to the classical contextual fear conditioning, but displayed increased escape behavior compared to males, suggesting an active response by females as opposed to freezing shown by males [42]. Interestingly, performance of female rats in the Y-maze version of the task was similar to those seen in males during the standard version of the task (although females had higher variability).…”

Section: Discussionsupporting

confidence: 92%

Exposure to variable prenatal stress in rats: Effects on anxiety-related behaviors, innate and contextual fear, and fear extinction

Wilson

Vazdarjanova

Terry

2013

Behavioural Brain Research

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Rats repeatedly exposed to variable prenatal stress (PNS) exhibit behavioral features often observed in neuropsychiatric disorders including elevated sensitivity to stimulants and impairments of attention, inhibitory control and memory-related task performance. However, to date there have been relatively few studies designed to assess the effects of PNS on anxiety, stress and fear responses, or the function of the hypothalamic-pituitary-adrenal (HPA) axis (a system clearly linked to stress and fear-related responses as well as neuropsychiatric disorders). In the current study, rats exposed to variable PNS were evaluated for anxiety-related behaviors in open field, elevated plus maze, and light/dark preference tasks. Innate fear responses were assessed using a predatory odor task and learned fear and extinction were assessed with a contextual fear conditioning task. As an indicator of HPA axis function, serum corticosterone levels were determined by enzyme immunoassay at various time points. The results indicated that PNS resulted in several behavioral anomalies including decreased innate fear responses to predator odor, impaired fear extinction, increased locomotor activity and stereotypic-like behaviors. Baseline levels of corticosterone in PNS subjects were similar to non-stressed controls; however, when exposed to acute stress, they exhibited an increase in corticosterone that was greater in magnitude. PNS was not associated with increased anxiety-like behaviors or deficits in learning or retention during contextual fear conditioning. Collectivity, these data support the argument that variable PNS in rats is a valid model system for studying some behavioral components of neuropsychiatric disorders as well as the influence of stress hormones.

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Section: Discussionsupporting

confidence: 92%

Exposure to variable prenatal stress in rats: Effects on anxiety-related behaviors, innate and contextual fear, and fear extinction

Wilson

Vazdarjanova

Terry

2013

Behavioural Brain Research

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“…Some studies report that females do not perform as well as males in fear conditioning and extinction learning (Baker-Andresen, Flavell, Li, & Bredy, 2013; Baran et al, 2009, 2010; Fenton et al, 2014). Male rats exhibit more freezing to the conditioned stimulus in fewer trials during fear conditioning compared to females (Aguilar et al, 2003; Baran et al, 2009, 2010; Daviu, Andero, Armario, & Nadal, 2014; Maren, De Oca, & Fanselow, 1994; Pryce, Lehmann, & Feldon, 1999; Ribeiro et al, 2010). Moreover, male rats trained to avoid an aversive arm (bright light and loud noise) in a plus maze, made more entries into the arm when the aversive stimuli were no longer present during extinction, while female rats decreased aversive arm exploration, indicating failure to extinguish the behavior (Ribeiro et al, 2010).…”

Section: Sex Differences In Fear Extinctionmentioning

confidence: 94%

“…Male rats exhibit more freezing to the conditioned stimulus in fewer trials during fear conditioning compared to females (Aguilar et al, 2003; Baran et al, 2009, 2010; Daviu, Andero, Armario, & Nadal, 2014; Maren, De Oca, & Fanselow, 1994; Pryce, Lehmann, & Feldon, 1999; Ribeiro et al, 2010). Moreover, male rats trained to avoid an aversive arm (bright light and loud noise) in a plus maze, made more entries into the arm when the aversive stimuli were no longer present during extinction, while female rats decreased aversive arm exploration, indicating failure to extinguish the behavior (Ribeiro et al, 2010). In a separate study, males performed better in a contextual fear conditioning task, while females expressed less fear and a higher extinction rate than males (Daviu et al, 2014).…”

Section: Sex Differences In Fear Extinctionmentioning

confidence: 94%

Sex differences in anxiety disorders: Interactions between fear, stress, and gonadal hormones

Maeng

Milad

2015

Hormones and Behavior

309

199

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Women are more vulnerable to stress- and fear-based disorders, such as anxiety and post-traumatic stress disorder. Despite the growing literature on this topic, the neural basis of these sex differences remains unclear, and the findings appear inconsistent. The neurobiological mechanisms of fear and stress in learning and memory processes have been extensively studied, and the crosstalk between these systems is beginning to explain the disproportionate incidence and differences in symptomatology and remission within these psychopathologies. In this review, we discuss the intersect between stress and fear mechanisms and their modulation by gonadal hormones and discuss the relevance of this information to sex differences in anxiety and fear-based disorders. Understanding these converging influences is imperative to the development of more effective, individualized treatments that take sex and hormones into account.

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“…While the sexual dimorphisms found in the brain structures (i.e., medial prefrontal cortex, amygdala, and hippocampus) that respond to stress and fear conditioning are thought to contribute to the sex differences seen in poor or adequate fear learning and extinction, results of preclinical and clinical studies have been mixed [27•]. Some, but not all [41], studies show male rats have superior fear conditioning and/or fear extinction, [e.g., 42, 43, 44, 45, 46] compared to female rats [47]. …”

Section: Sex Differences In the Physiologic Response To Traumamentioning

confidence: 99%

What Does Sex Have to Do with It? The Role of Sex as a Biological Variable in the Development of Posttraumatic Stress Disorder

Kornfield

Hantsoo

Epperson

2018

Curr Psychiatry Rep

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While others have suggested that trauma type or acute emotional reaction are responsible for women's disproportionate risk to PTSD, neither of these explanations fully accounts for the sex differences in PTSD. Sex differences in brain neurocircuitry, anatomy, and neurobiological processes, such as those involved in learning and memory, are discussed as they have been implicated in risk and resilience for the development of PTSD. Gonadal and stress hormones have been found to modulate sex differences in the neurocircuitry and neurochemistry underlying fear learning and extinction. Preclinical research has not consistently controlled for hormonal and reproductive status of rodents nor have clinical studies consistently examined these factors as potential moderators of risk for PTSD. Sex as a biological variable (SABV) should be considered, in addition to the endocrine and reproductive status of participants, in all stress physiology and PTSD research.

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Sex differences in aversive memory in rats: Possible role of extinction and reactive emotional factors

Cited by 49 publications

References 42 publications

Exposure to variable prenatal stress in rats: Effects on anxiety-related behaviors, innate and contextual fear, and fear extinction

Exposure to variable prenatal stress in rats: Effects on anxiety-related behaviors, innate and contextual fear, and fear extinction

Sex differences in anxiety disorders: Interactions between fear, stress, and gonadal hormones

What Does Sex Have to Do with It? The Role of Sex as a Biological Variable in the Development of Posttraumatic Stress Disorder

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