Ellis Seneca N, Honeycutt Jennifer A
Program in Neuroscience, Bowdoin College, Brunswick, ME, United States.
Department of Psychology, Bowdoin College, Brunswick, ME, United States.
Front Behav Neurosci. 2021 Nov 4;15:741454. doi: 10.3389/fnbeh.2021.741454. eCollection 2021.
The early life environment markedly influences brain and behavioral development, with adverse experiences associated with increased risk of anxiety and depressive phenotypes, particularly in females. Indeed, early life adversity (ELA) in humans (i.e., caregiver deprivation, maltreatment) and rodents (i.e., maternal separation, resource scarcity) is associated with sex-specific emergence of anxious and depressive behaviors. Although these disorders show clear sex differences in humans, little attention has been paid toward evaluating sex as a biological variable in models of affective dysfunction; however, recent rodent work suggests sex-specific effects. Two widely used rodent models of ELA approximate caregiver deprivation (i.e., maternal separation) and resource scarcity (i.e., limited bedding). While these approaches model aspects of ELA experienced in humans, they span different portions of the pre-weaning developmental period and may therefore differentially contribute to underlying mechanistic risk. This is borne out in the literature, where evidence suggests differences in trajectories of behavior depending on the type of ELA and/or sex; however, the neural underpinning of these differences is not well understood. Because anxiety and depression are thought to involve dysregulation in the balance of excitatory and inhibitory signaling in ELA-vulnerable brain regions (e.g., prefrontal cortex, amygdala, hippocampus), outcomes are likely driven by alterations in local and/or circuit-specific inhibitory activity. The most abundant GABAergic subtypes in the brain, accounting for approximately 40% of inhibitory neurons, contain the calcium-binding protein Parvalbumin (PV). As PV-expressing neurons have perisomatic and proximal dendritic targets on pyramidal neurons, they are well-positioned to regulate excitatory/inhibitory balance. Recent evidence suggests that PV outcomes following ELA are sex, age, and region-specific and may be influenced by the type and timing of ELA. Here, we suggest the possibility of a combined role of PV and sex hormones driving differences in behavioral outcomes associated with affective dysfunction following ELA. This review evaluates the literature across models of ELA to characterize neural (PV) and behavioral (anxiety- and depressive-like) outcomes as a function of sex and age. Additionally, we detail a putative mechanistic role of PV on ELA-related outcomes and discuss evidence suggesting hormone influences on PV expression/function which may help to explain sex differences in ELA outcomes.
早期生活环境对大脑和行为发育有显著影响,不良经历会增加焦虑和抑郁表型的风险,尤其是在女性中。事实上,人类(即照顾者剥夺、虐待)和啮齿动物(即母婴分离、资源匮乏)的早期生活逆境(ELA)与焦虑和抑郁行为的性别特异性出现有关。尽管这些疾病在人类中表现出明显的性别差异,但在情感功能障碍模型中,很少有人关注将性别作为一个生物学变量进行评估;然而,最近的啮齿动物研究表明存在性别特异性效应。两种广泛使用的ELA啮齿动物模型分别模拟照顾者剥夺(即母婴分离)和资源匮乏(即垫料有限)。虽然这些方法模拟了人类经历的ELA的各个方面,但它们跨越了断奶前发育阶段的不同部分,因此可能对潜在的机制风险有不同的贡献。这在文献中得到了证实,有证据表明,根据ELA的类型和/或性别,行为轨迹存在差异;然而,这些差异的神经基础尚不清楚。因为焦虑和抑郁被认为与ELA易损脑区(如前额叶皮质、杏仁核、海马体)兴奋性和抑制性信号平衡的失调有关,其结果可能是由局部和/或特定回路的抑制活性改变所驱动的。大脑中最丰富的GABA能亚型约占抑制性神经元的40%,含有钙结合蛋白小白蛋白(PV)。由于表达PV的神经元在锥体神经元上有胞体周围和近端树突靶点,它们处于调节兴奋/抑制平衡的有利位置。最近的证据表明,ELA后的PV结果具有性别、年龄和区域特异性,可能受ELA的类型和时间影响。在这里,我们提出PV和性激素共同作用导致ELA后与情感功能障碍相关的行为结果差异的可能性。本综述评估了ELA模型的文献,以表征神经(PV)和行为(焦虑样和抑郁样)结果与性别和年龄的关系。此外,我们详细阐述了PV对ELA相关结果的假定机制作用,并讨论了表明激素对PV表达/功能有影响的证据,这可能有助于解释ELA结果中的性别差异。