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It is well documented that synaptotoxic soluble amyloid-\u03b2 aggregates facilitate synaptic long-term depression, a major form of synaptic weakening that correlates with cognitive status in Alzheimer\u2019s disease. Whether synaptotoxic tau, which is also associated strongly with progressive cognitive decline in patients with Alzheimer\u2019s disease and other tauopathies, also causes facilitation remains to be clarified. Young male adult and middle-aged rats were employed. Synaptotoxic tau and amyloid-\u03b2 were obtained from different sources including (i) aqueous brain extracts from patients with Alzheimer\u2019s disease and Pick\u2019s disease tauopathy; (ii) the secretomes of induced pluripotent stem cell-derived neurons from individuals with trisomy of chromosome 21; and (iii) synthetic amyloid-\u03b2. In vivo electrophysiology was performed in urethane anaesthetized animals. Evoked field excitatory postsynaptic potentials were recorded from the stratum radiatum in the CA1 area of the hippocampus with electrical stimulation to the Schaffer collateral\u2013commissural pathway. To study the enhancement of long-term depression, relatively weak low-frequency electrical stimulation was used to trigger peri-threshold long-term depression. Synaptotoxic forms of tau or amyloid-\u03b2 were administered intracerebroventricularly. The ability of agents that inhibit the cytokine tumour necrosis factor-\u03b1 or the integrated stress response to prevent the effects of amyloid-\u03b2 or tau on long-term depression was assessed after local or systemic injection, respectively. We found that diffusible tau from Alzheimer\u2019s disease or Pick\u2019s disease patients\u2019 brain aqueous extracts or the secretomes of trisomy of chromosome 21 induced pluripotent stem cell-derived neurons, like Alzheimer\u2019s disease brain-derived amyloid-\u03b2 and synthetic oligomeric amyloid-\u03b2, potently enhanced synaptic long-term depression in live rats. We further demonstrated that long-term depression facilitation by both tau and amyloid-\u03b2 was age-dependent, being more potent in middle-aged compared with young animals. Finally, at the cellular level, we provide pharmacological evidence that tumour necrosis factor-\u03b1 and the integrated stress response are downstream mediators of long-term depression facilitation by both synaptotoxic tau and amyloid-\u03b2. Overall, these findings reveal the promotion of an age-dependent synaptic weakening by both synaptotoxic tau and amyloid-\u03b2. Pharmacologically targeting shared mechanisms of tau and amyloid-\u03b2 synaptotoxicity, such as tumour necrosis factor-\u03b1 or the integrated stress response, provides an attractive strategy to treat early Alzheimer\u2019s disease.<\/jats:p>","DOI":"10.1093\/braincomms\/fcae333","type":"journal-article","created":{"date-parts":[[2024,9,27]],"date-time":"2024-09-27T11:32:31Z","timestamp":1727436751000},"source":"Crossref","is-referenced-by-count":10,"title":["Patient-derived tau and amyloid-\u03b2 facilitate long-term depression <i>in vivo<\/i>: role of tumour necrosis factor-\u03b1 and the integrated stress response"],"prefix":"10.1093","volume":"6","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5571-296X","authenticated-orcid":false,"given":"Neng-Wei","family":"Hu","sequence":"first","affiliation":[{"name":"Department of Pharmacology & Therapeutics, School of Medicine, and Institute of Neuroscience, Trinity College , Dublin 2, Dublin ,","place":["Ireland"]},{"name":"Department of Physiology and Neurobiology, School of Basic Medical Sciences, Zhengzhou University , Zhengzhou 450001 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomas","family":"Ondrejcak","sequence":"additional","affiliation":[{"name":"Department of Pharmacology & Therapeutics, School of Medicine, and Institute of Neuroscience, Trinity College , Dublin 2, Dublin ,","place":["Ireland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Igor","family":"Klyubin","sequence":"additional","affiliation":[{"name":"Department of Pharmacology & Therapeutics, School of Medicine, and Institute of Neuroscience, Trinity College , Dublin 2, Dublin ,","place":["Ireland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yin","family":"Yang","sequence":"additional","affiliation":[{"name":"Department of Pharmacology & Therapeutics, School of Medicine, and Institute of Neuroscience, Trinity College , Dublin 2, Dublin ,","place":["Ireland"]},{"name":"Department of Physiology and Neurobiology, School of Basic Medical Sciences, Zhengzhou University , Zhengzhou 450001 ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dominic M","family":"Walsh","sequence":"additional","affiliation":[{"name":"Laboratory for Neurodegenerative Research, Ann Romney Center for Neurologic Diseases, Brigham and Women\u2019s Hospital and Harvard Medical School , Boston, MA 02115 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frederick J","family":"Livesey","sequence":"additional","affiliation":[{"name":"UCL Great Ormond Street Institute of Child Health, Zayed Centre for Research into Rare Disease in Children, University College London , London WC1N 1DZ ,","place":["UK"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael J","family":"Rowan","sequence":"additional","affiliation":[{"name":"Department of Pharmacology & Therapeutics, School 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