Department of Psychiatry, Harvard Medical School and McLean Hospital, Belmont, MA 02478, United States.
Department of Psychiatry, Harvard Medical School and McLean Hospital, Belmont, MA 02478, United States.
Neurobiol Learn Mem. 2019 Jan;157:24-34. doi: 10.1016/j.nlm.2018.11.011. Epub 2018 Nov 17.
The stress-related neuropeptide pituitary adenylate cyclase-activating polypeptide (PACAP) is implicated in neuromodulation of learning and memory. PACAP can alter synaptic plasticity and has direct actions on neurons in the amygdala and hippocampus that could contribute to its acute and persistent effects on the consolidation and expression of conditioned fear. We recently demonstrated that intracerebroventricular (ICV) infusion of PACAP prior to fear conditioning (FC) results in initial amnestic-like effects followed by hyper-expression of conditioned freezing with repeated testing, and analyses of immediate-early gene c-Fos expression suggested that the central nucleus of the amygdala (CeA), but not the lateral/basolateral amygdala (LA/BLA) or hippocampus, are involved in these PACAP effects. Here, we extend that work by examining the expression of the synaptic plasticity marker activity-regulated cytoskeleton-associated protein (Arc/Arg 3.1) after PACAP administration and FC. Male Sprague-Dawley rats were implanted with cannula for ICV infusion of PACAP-38 (1.5 µg) or vehicle followed by FC and tests for conditioned freezing. One hour after FC, Arc protein expression was significantly elevated in the CeA and bed nucleus of the stria terminalis (BNST), interconnected structures that are key elements of the extended amygdala, in rats that received the combination of PACAP + FC. In contrast, Arc expression within the subdivisions of the hippocampus, or the LA/BLA, were unchanged. A subpopulation of Arc-positive cells in both the CeA and BNST also express PKCdelta, an intracellular marker that has been used to identify microcircuits that gate conditioned fear in the CeA. Consistent with our previous findings, on the following day conditioned freezing behavior was reduced in rats that had been given the combination of PACAP + FC-an amnestic-like effect-and Arc expression levels had returned to baseline. Given the established role of Arc in modifying synaptic plasticity and memory formation, our findings suggest that PACAP-induced overexpression of Arc following fear conditioning may disrupt neuroplastic changes within populations of CeA and BNST neurons normally responsible for encoding fear-related cues that, in this case, results in altered fear memory consolidation. Hence, PACAP systems may represent an axis on which stress and experience-driven neurotransmission converge to alter emotional memory, and mediate pathologies that are characteristic of psychiatric illnesses such as post-traumatic stress disorder.
应激相关神经肽垂体腺苷酸环化酶激活肽(PACAP)参与学习和记忆的神经调节。PACAP 可以改变突触可塑性,并直接作用于杏仁核和海马中的神经元,这可能有助于其对条件性恐惧的巩固和表达产生急性和持续的影响。我们最近的研究表明,在恐惧条件化(FC)之前,通过脑室内(ICV)输注 PACAP 会导致初始健忘样效应,随后在重复测试时出现条件性冻结的过度表达,并且即时早期基因 c-Fos 表达的分析表明,杏仁核中央核(CeA),而不是外侧/基底杏仁核(LA/BLA)或海马体,参与了这些 PACAP 效应。在这里,我们通过检查 PACAP 给药和 FC 后突触可塑性标记物活性调节细胞骨架相关蛋白(Arc/Arg3.1)的表达来扩展该工作。雄性 Sprague-Dawley 大鼠被植入用于脑室内输注 PACAP-38(1.5μg)或载体的导管,然后进行 FC 和条件性冻结测试。FC 后 1 小时,在接受 PACAP+FC 联合治疗的大鼠的 CeA 和终纹床核(BNST)中,Arc 蛋白表达显著升高,这是扩展杏仁核的关键结构。相比之下,海马体或 LA/BLA 内的亚区的 Arc 表达没有变化。CeA 和 BNST 中的 Arc 阳性细胞亚群也表达 PKCdelta,PKCdelta 是一种细胞内标志物,用于识别 CeA 中门控条件性恐惧的微电路。与我们之前的发现一致,在接受 PACAP+FC 联合治疗的大鼠中,第二天的条件性冻结行为减少了-一种健忘样效应-并且 Arc 表达水平已恢复到基线。鉴于 Arc 在修饰突触可塑性和记忆形成中的既定作用,我们的研究结果表明,恐惧条件化后 PACAP 诱导的 Arc 过度表达可能会破坏 CeA 和 BNST 神经元群体内通常负责编码与恐惧相关线索的神经可塑性变化,在这种情况下,会导致恐惧记忆巩固的改变。因此,PACAP 系统可能代表了应激和经验驱动的神经传递汇聚以改变情绪记忆的轴,并介导创伤后应激障碍等精神疾病的特征性病理学。