The Type 3 Adenylyl Cyclase Is Required for Novel Object Learning and Extinction of Contextual Memory: Role of cAMP Signaling in Primary Cilia
Open accessAbstract
Although primary cilia are found on neurons throughout the brain, their physiological function remains elusive. Human ciliopathies are associated with cognition defects, and transgenic mice lacking proteins expressed in primary cilia exhibit defects in learning and memory. Recently, it was reported that mice lacking the G-protein-coupling receptor somatostatin receptor-3 (SSTR3), a protein expressed predominately in the primary cilia of neurons, have defective memory for novel object recognition and lower cAMP levels in the brain. Since SSTR3 is coupled to regulation of adenylyl cyclase, this suggests that adenylyl cyclase activity in primary cilia of CNS neurons may be critical for some forms of learning and memory. Because the type 3 adenylyl cyclase (AC3) is expressed in primary cilia of hippocampal neurons, we examined AC3 −/− mice for several forms of learning and memory. Here, we report that AC3 −/− mice show no short-term memory for novel objects and fail to exhibit extinction of contextual fear conditioning. They also show impaired learning and memory for temporally dissociative passive avoidance. Since AC3 is exclusively expressed in primary cilia, we conclude that cAMP signals generated within primary cilia contribute to some forms of learning and memory, including extinction of contextual fear conditioning.
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Knockout of AC3 impairs memory for temporally dissociative passive avoidance but does not affect contextual fear memory and short-term memory for novel object recognition.
“Knockout of AC3 impairs memory for temporally dissociative passive avoidance but does not affect contextual fear memory and short-term memory for novel object recognition (Wang et al., 2011).”
From Primary cilia in the mature brain: emerging roles in Alzheimer's disease pathogenesis (2025) · cites this paper as Wang et al., 2011
The Results sections on TDPA and contextual fear conditioning support the claimed TDPA impairment and intact contextual fear memory. But the Results section on novel object recognition states the opposite of the final clause: AC3−/− mice showed no preference for the novel object after 5 minutes, indicating impaired short-term recognition memory. (LLM, conf=0.89)
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Experimental — accuracy not yet measuredGenetic ablation of both AC3 and SSTR3 significantly impacts several region-related functions, including specific forms of memory.
“Previous research has demonstrated that SSTR3-induced signalling is associated with AC in the hippocampus (Einstein et al. 2010), and the genetic ablation of both AC3 and SSTR3 significantly impacts several region-related functions, including specific forms of memory (Wang, Phan, and Storm 2011;Chen et al. 2016;Wang et al. 2025).”
From Changes of the Primary Cilia in Alzheimer's Disease Pathogenesis (2025) · cites this paper as Wang, Phan, and Storm 2011
The Discussion reports that separate AC3−/− and SSTR3−/− mice are both deficient in novel-object memory. It also reports several learning and memory deficits in AC3−/− mice, but does not establish that SSTR3 ablation affects several functions or that both genes were ablated together. (LLM, conf=0.84)
Experimental — accuracy not yet measuredNeuronal cilia may house signaling cascades critical for learning and memory and therefore may be important in AD pathogenesis.
“These findings suggest that neuronal cilia may house signaling cascades critical for learning and memory [43, 44] and therefore, may be important in AD pathogenesis.”
From Amyloid-β interrupts canonical Sonic hedgehog signaling by distorting primary cilia structure (2018) · cites this paper as [44]
In the hippocampus of adult (3-8 months old) male mice, AC3-labeled primary cilia are abundant in the pyramidal cell layers of the CA1 and CA3 regions, as well as in the granular cell layer of the dentate gyrus.
“In the hippocampus of adult (3–8 months old) male mice, AC3-labeled primary cilia are abundant in the pyramidal cell layers of the CA1 and CA3 regions, as well as in the granular cell layer of the dentate gyrus (DG) (Wang et al., 2011).”
From Primary cilia in the mature brain: emerging roles in Alzheimer's disease pathogenesis (2025) · cites this paper as Wang et al., 2011
Conditional disruption of cilia in adult mice causes hyperphagia and obesity.
“conditional disruption of cilia in adult mice causes hyperphagia and obesity 177, 178.”
From Cellular signalling by primary cilia in development, organ function and disease (2019) · cites this paper as [177]
The Materials and Methods (Mice; page unavailable) describe adult AC3-deficient mice, but not conditional disruption of cilia. The paper’s findings concern learning and memory; searches for hyperphagia and obesity found no passage reporting the claimed effect. Obesity appears only in the title of a different work listed in References (page unavailable). (LLM, conf=0.77)
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- Authors
- Wang, Z., Phan, T., & Storm, D. R.
- Affiliations
- Hebei University (CN)
- University of Washington (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-04-13
- Volume
- 31
- Issue
- 15
- Pages
- 5557-5561
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3091825
- OpenAlex
- W2010458044
- Cited by
- 100
- References
- 35
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 3 · 2023: 4 · 2022: 7 · 2021: 13 · 2020: 7 · 2019: 6 · 2018: 6 · 2017: 9 · 2016: 6 · 2015: 7 · 2014: 10 · 2013: 4 · 2012: 8
- FWCI
- 3.74
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5t32gm007108-40, GM07108, T32 GM07108)
- National Institute of Mental Health (MH 073601, R01MH073601)
- National Institute on Deafness and Other Communication Disorders (R01DC004156)
- National Institute of General Medical Sciences (5 T32-GM07108, T32GM-007108)
- National Institute of Neurological Disorders and Stroke (R01NS020498, NS020498)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Kidney Cyst Diseases
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- primary cilia, cAMP signaling, novel object recognition, contextual fear conditioning, fear extinction, passive avoidance, learning and memory, hippocampal neurons, ciliopathies, SSTR3
- MeSH terms
- Cyclic AMP, Adenylyl Cyclases, Animals, Avoidance Learning, Cilia, Extinction, Psychological, Fear, Hippocampus, Immunohistochemistry, Learning, Memory, Memory Disorders, Memory, Short-Term, Mice, Inbred C57BL, Signal Transduction, Mice, Knockout, Recognition, Psychology, Mice, Memory, Long-Term
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