Manipulation of hippocampal CA3 firing via luminopsins modulates spatial and episodic short-term memory, especially working memory, but not long-term memory

Song, Da; Yang, Qinghu; Lang, Yiran; Wen, Zhaosen; Xie, Zhen; Zheng, Da-Zhong; Yan, Tianyi; Deng, Yujun; Nakanishi, Hiroshi; Quan, Zhenzhen; Qing, Hong

doi:10.1016/j.nlm.2018.09.009

Cited by 19 publications

(15 citation statements)

References 43 publications

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“…To accommodate the need for non-invasive stimulation of genetically targeted neural circuits in a postnatally growing brain and temporally precise interrogation of the same circuits in the same animal as an adult, we employed bioluminescent optogenetics (BL-OG) (Berglund et al, 2013(Berglund et al, , 2016Park et al, 2017;Song et al, 2018;Zenchak et al, 2018;Gomez-Ramirez et al, 2019;Yu et al, 2019). Here an optogenetic element can be activated either by light emitted from a tethered luciferase oxidizing a small molecule substrate, or by light emitted from physical sources, such as LEDs or lasers ( Figure 1A).…”

Section: Bioluminescent Optogenetics Allows Developmental Chemogenetimentioning

confidence: 99%

Selective Postnatal Excitation of Neocortical Pyramidal Neurons Results in Distinctive Behavioral and Circuit Deficits in Adulthood

Medendorp

Pal

Waddell

et al. 2020

Preprint

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In leading models of Autism Spectrum Disorder, and in human data, the efficacy of outgoing cortical connectivity transitions from overly exuberant to languid from early development to adulthood. This transition begs the question of whether the early enhancement in excitation might be a common driver, across etiologies, of these symptoms. We directly tested this concept by chemogenetically driving neuronal activity in neocortical neurons during postnatal days 4-14. Hyperexcitation of Emx1-, but not dopamine transporter-, parvalbumin-, or Dlx5/6-expressing neurons led to decreased social interaction and increased grooming activity in adult animals. In vivo optogenetic interrogation in adults revealed decreased baseline but increased stimulus-evoked firing rates of pyramidal neurons, impaired recruitment of inhibitory neurons and reduced cortico-striatal communication. These results directly support the prediction that changed firing in developing circuits irreversibly alters adult circuit function that leads to maladaptive changes in behaviors. This experimental approach offers a valuable platform to study the impact of disruption of developmental neural activity on the formation and function of adult neural circuits and behavior.

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Section: Bioluminescent Optogenetics Allows Developmental Chemogenetimentioning

confidence: 99%

Selective Postnatal Excitation of Neocortical Pyramidal Neurons Results in Distinctive Behavioral and Circuit Deficits in Adulthood

Medendorp

Pal

Waddell

et al. 2020

Preprint

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“…It is found that mice with higher neurogenesis show relatively lower depression symptoms and stronger social interactions compared with the control group ( Song et al., 2018 ). Stress factors could reduce the incidence of adult neurogenesis.…”

Section: Discussionmentioning

confidence: 99%

“…RR036A, TaKaRa). The PCR step was as follows: 1 cycle at 95°C for 3 min; 39 cycles at 95°C for 10 s, and 60°C for 30 s ( Song et al., 2018 ).…”

Section: Methodsmentioning

confidence: 99%

The Anti-Depression-Like Effects of Zhengtian Capsule via Induction of Neurogenesis and the Neurotrophic Signaling Pathway

Yang

Wang

et al. 2020

Front. Pharmacol.

Self Cite

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Oxidative stress that causes neural damages in neurodegenerative disorders has been widely studied for the pathogenesis and diagnostic measures. Zhengtian capsule (ZTC), a type of traditional Chinese medicine for headaches, has been found to have extra effects in recent years, such as promoting the release of serotonin and dopamine in the brain, but its specific mechanism has not been clearly elucidated. In this study, we focus on revealing whether ZTC can regulate key proteins of neurotrophic signaling pathway to alleviate depression-like behavior caused by oxidative stress. Experimental results show that ZTC (M 0.34 and H 0.7 g/kg) can elevate the proliferation of neural stem cells and GABAergictype neurons in the hippocampus, promote the protein levels of BDNF, phosphorylated ERK1/2, and CREB, and inhibit the expression level of a key inflammation factor NFkB in a dose-dependent manner. These data suggest ZTC acts on multiple pathways to resist excessive oxidative stress, proving it to be a potential neurotrophic drug.

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“…Namely, within the CA3 area, but not in the cingulate and motor cortex, c-fos expression was important for spatial memory formation when tested in a radial arm maze [He et al, 2002]. At the same time, it was shown that excitation or inhibition of neurons within the CA3 hippocampal area led to impaired spatial working memory in the T-maze [Song et al, 2018], and blocking of SNAP-25 protein production in the CA3 hippocampal area resulted in impaired spatial and long-term memory [Hou et al, 2006]. Current ideas about the role of the CA3 hippocampal area in the implementation of cognitive functions suggest the significance of dendritic characteristics of CA3 pyramidal neurons in memory storage and recall [Kaifosh and Losonczy, 2016].…”

Section: Discussionmentioning

confidence: 99%

Neuropathic Pain Causes a Decrease in the Dendritic Tree Complexity of Hippocampal CA3 Pyramidal Neurons

Tyrtyshnaia

Manzhulo

Konovalova

et al. 2019

Cells Tissues Organs

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The International Pain Association defines neuropathic pain as "an unpleasant sensory and emotional experience associated with actual or potential tissue damage." Recent studies show that chronic neuropathic pain causes both morphological and functional changes within brain structures. Due to the impact of supraspinal centers on pain signal processing, patients with chronic pain often suffer from depression, anxiety, memory impairment, and learning disabilities. Changes in hippocampal neuronal and glial plasticity can play a substantial role in the development of these symptoms. Given the special role of the CA3 hippocampal area in chronic stress reactions, we suggested that this region may undergo significant morphological changes as a result of persistent pain. Since the CA3 area is involved in the implementation of hippocampus-dependent memory, changes in the neuronal morphology can cause cognitive impairment observed in chronic neuropathic pain. This study aimed to elucidate the structural and plastic changes within the hippocampus associated with dendritic tree atrophy of CA3 pyramidal neurons in mice with chronic sciatic nerve constric-tion. Behavioral testing revealed impaired working and long-term memory in mice with a chronic constriction injury. Using the Golgi-Cox method, we revealed a decrease in the number of branches and dendritic length of CA3 pyramidal neurons. The dendritic spine number was decreased, predominantly due to a reduction in mushroom spines. An immunohistochemical study showed changes in astro-and microglial activity, which could affect the morphology of neurons both directly and indirectly via the regulation of neurotrophic factor synthesis. Using ELISA, we found a decrease in brain-derived neurotrophic factor production and an increase in neurotrophin-3 production. Morphological and biochemical changes in the CA3 area are accompanied by impaired working and long-term memory of animals. Thus, we can conclude that morphological and biochemical changes within the CA3 hippocampal area may underlie the cognitive impairment in neuropathic pain.

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Manipulation of hippocampal CA3 firing via luminopsins modulates spatial and episodic short-term memory, especially working memory, but not long-term memory

Cited by 19 publications

References 43 publications

Selective Postnatal Excitation of Neocortical Pyramidal Neurons Results in Distinctive Behavioral and Circuit Deficits in Adulthood

Selective Postnatal Excitation of Neocortical Pyramidal Neurons Results in Distinctive Behavioral and Circuit Deficits in Adulthood

The Anti-Depression-Like Effects of Zhengtian Capsule via Induction of Neurogenesis and the Neurotrophic Signaling Pathway

Neuropathic Pain Causes a Decrease in the Dendritic Tree Complexity of Hippocampal CA3 Pyramidal Neurons

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