Cited by 136Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

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Selective cognitive dysfunction in mice lacking histamine H1 and H2 receptors

Dai, Hongmei, Kaneko, Kenya, Kato, Hiroshi, Fujii, Satoshi, Jing, Yuhong, Xu, Ajing, Sakurai, Eiko, Kato, Motohisa, Okamura, Nobuyuki, Kuramasu, Atsuo, Yanai, Kazuhiko·2007·Neuroscience Research

DOI 10.1016/j.neures.2006.10.020

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Abstract

Previous pharmacological experiments provide conflicting findings that describe both facilitatory and inhibitory effects of neuronal histamine on learning and memory. Here, we examined learning and memory and synaptic plasticity in mice with a null mutation of gene coding histamine H1 or H2 receptor in order to clarify the role of these receptors in learning and memory processes. Learning and memory were evaluated by several behavioral tasks including object recognition, Barnes maze and fear conditioning. These behavioral tasks are highly dependent on the function of prefrontal cortex, hippocampus or amygdala. Object recognition and Barnes maze performance were significantly impaired in both H1 receptor gene knockout (H1KO) and H2 receptor gene knockout (H2KO) mice when compared to the respective wild-type (WT) mice. Conversely, both H1KO and H2KO mice showed better auditory and contextual freezing acquisition than their respective WT mice. Furthermore, we also examined long-term potentiation (LTP) in the CA1 area of hippocampus in H1KO and H2KO mice and their respective WT mice. LTP in the CA1 area of hippocampus was significantly reduced in both H1KO and H2KO mice when compared with their respective WT mice. In conclusion, our results demonstrate that both H1 and H2 receptors are involved in learning and memory processes for which the frontal cortex, amygdala and hippocampus interact.

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BackgroundMethodInfluential
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Background
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BackgroundResultInfluential
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Background
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Background
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“In contrast, inhibitory avoidance and short-term object place recognition seem to be not affected in these mice (Yanai et al., 1998; Zlomuzica et al., 2008) and contextual fear conditioning is even improved compared to WT mice (Dai et al., 2007).”
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Background
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“campal cornu ammonis-1 area (Dai et al., 2007).”
Background
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Background
Redundant Catecholamine Signaling Consolidates Fear Memory via Phospholipase C
Ouyang, M., Young, M. B., Lestini, M. M., Schutsky, K., & THOMAS, S. A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5231-11.2012 · Cited by 26
“…serotonergic receptor 5-HT2a or 5-HT2c, adrenergic receptor 1d, or histaminergic receptor H1 all exhibit intact cued fear memory (Aiba et al., 1994; Lu et al., 1997; Tecott et al., 1998; Anagnostaras et al., 2003; Sadalge et al., 2003; Weisstaub et al., 2006; Dai et al., 2007; Poulin et al., 2010).”
Background
Involvement of histamine 1 receptor in seizure susceptibility and neuroprotection in immature mice
Kukko‐Lukjanov, T., Lintunen, M., Jalava, N., Laurén, H. B., Lopez‐Picon, F. R., Michelsen, K. A., Panula, P., & Holopainen, I. E. (2010) · Epilepsy Research · doi:10.1016/j.eplepsyres.2010.02.012 · Cited by 26
Motivated exploratory behaviour in the rat: The role of hippocampus and the histaminergic neurotransmission
Alvarez, E. O., & Alvarez, P. A. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.07.038 · Cited by 25
Histamine Receptor Expression, Hippocampal Plasticity and Ammonia in Histidine Decarboxylase Knockout Mice
Chepkova, A. N., Yanovsky, E., Parmentier, R., Ohtsu, H., Haas, H. L., Lin, J., & Sergeeva, O. A. (2011) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-011-9730-1 · Cited by 25
Point‐of‐Care Health Diagnostics and Food Quality Monitoring by Molecularly Imprinted Polymers‐Based Histamine Sensors
Ahmed, S., Ansari, A., Li, Z., Mazumdar, H., Siddiqui, M. A., Khan, A., Ranjan, P., Kaushik, A. K., Vinu, A., & Kumar, P. (2024) · Advanced Sensor Research · doi:10.1002/adsr.202400132 · Cited by 26
Effect of Noise and Music on Neurotransmitters in the Amygdala: The Role Auditory Stimuli Play in Emotion Regulation
Nian, H., Ding, S., Feng, Y., Liu, H., Li, J., Li, X., Zhang, R., & Bao, J. (2023) · Metabolites · doi:10.3390/metabo13080928 · Cited by 24
“Histidine is the precursor of histamine in the central nervous system (CNS) [31], and histidine de-carboxylation is one of the most important sources of histamine [32].”
Background
Context-Dependent Effects of a Single Administration of Mirtazapine on the Expression of Methamphetamine-Induced Conditioned Place Preference
Voigt, R. M., & Napier, T. C. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00092 · Cited by 23
Exploring the mediation of DNA methylation across the epigenome between childhood adversity and First Episode of Psychosis—findings from the EU-GEI study
Alameda, L., Liu, Z., Sham, P. C., Aas, M., Trotta, G., Rodríguez, V., Forti, M. D., Stilo, S. A., Kandaswamy, R., Arango, C., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02044-9 · Cited by 24
“Lastly, low overlap between mediating genes and pathways according to abuse and neglect suggests that biological trajectories between CA and psychosis are distinct depending on the type of adversity.”
Background
Identification of histaminergic neurons through histamine 3 receptor-mediated autoinhibition
Luca, R. D., Suvorava, T., Yang, D., Baumgärtel, W., Kojda, G., Haas, H. L., & Sergeeva, O. A. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.08.025 · Cited by 23
Histamine: A Key Neuromodulator of Memory Consolidation and Retrieval
Nomura, H., Shimizume, R., & Ikegaya, Y. (2021) · Current topics in behavioral neurosciences · doi:10.1007/7854_2021_253 · Cited by 22
“However, both H1R- and H2R-deficient mice show greater conditioned fear responses than wildtype mice in the fear conditioning test (Dai et al. 2007).”
BackgroundResult
Impact of moderate prenatal alcohol exposure on histaminergic neurons, histidine decarboxylase levels and histamine H2 receptors in adult rat offspring
Davies, S., Ballesteros‐Merino, C., Allen, N. A., Porch, M. W., Pruitt, M. E., Christensen, K. H., Rosenberg, M. J., & Savage, D. D. (2018) · Alcohol · doi:10.1016/j.alcohol.2018.07.007 · Cited by 22
Histamine H1 receptor antagonist cetirizine impairs working memory processing speed, but not episodic memory
van Ruitenbeek, P., Vermeeren, A., & Riedel, W. J. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00907.x · Cited by 22
“On the one hand, recent studies have shown that H1-recepter knockout animals and H2-receptor knockout animals performed worse on maze tasks and object recognition as compared with wild-type mice (Dai et al., 2007; Zlomuzica et al., 2009), which suggests a memory promoting role for histamine.”
The activation of histamine-sensitive sites of the ventral hippocampus modulates the consolidation of a learned active avoidance response in rats
Alvarez, E. O., & Banzán, A. M. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.12.015 · Cited by 21
Emotional memory consolidation impairment induced by histamine is mediated by H1 but not H2 receptors
Gianlorenço, A. C., Serafim, K. R., Canto‐de‐Souza, A., & Mattioli, R. (2012) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2012.09.003 · Cited by 20
Persistent activation of histamine H1 receptors in the hippocampal CA1 region enhances NMDA receptor-mediated synaptic excitation and long-term potentiation in astrocyte- and D-serine-dependent manner
Masuoka, T., Ikeda, R., & Konishi, S. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.03.036 · Cited by 20
“For example, spatial reference and working memory is impaired in H1 receptor knockout mice, probably through deficits in synaptic plasticity in the hippocampus caused by changes in cholinergic neurochemical parameters in the frontal cortex and hippocampal CA1 region (Dai et al., 2007).”
AMELIORATIVE EFFECTS OF HISTAMINE ON SPATIAL MEMORY DEFICITS INDUCED BY SCOPOLAMINE INFUSION INTO BILATERAL DORSAL OR VENTRAL HIPPOCAMPUS AS EVALUATED BY THE RADIAL ARM MAZE TASK
Xu, L., Fan, Y., He, P., Zhang, W., Hu, W., & Chen, Z. (2009) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2009.05157.x · Cited by 19
“recently reported that object recognition and Barnes maze performance were significantly impaired in both H1 and H2 receptor gene knockout mice compared with their respective wild-type counterparts.(34) Bilateral post-training injection of the histamine H2 agonist amthamine into the DH improved memory consolidation.”
Background
Overexpression of Type I Adenylyl Cyclase in the Forebrain Impairs Spatial Memory in Aged But Not Young Mice
Garelick, M. G., Chan, G. C. K., DiRocco, D. P., & Storm, D. R. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0553-09.2009 · Cited by 18
“We used a paradigm with multiple training sessions per day modified from Dai et al. (2007).”
Method
Endogenous Histamine Facilitates Long-Term Potentiation in the Hippocampus during Walking
Luo, T., & Leung, L. S. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1127-10.2010 · Cited by 24
“LTP of the Schaffer collateral (presumed apical dendritic) synapses in CA1 in vitro was reduced in H1 and H2 receptor gene knock-out mice (Dai et al., 2007), but potentiation of population spikes was enhanced in mice lacking histidine decarboxylase, the enzyme responsible for the synthesis of histamine (Liu et al.”
Background
Suggesting a possible role of CA1 histaminergic system in harmane-induced amnesia
Nasehi, M., Mashaghi, E., Khakpai, F., & Zarrindast, M. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.09.066 · Cited by 17
The Role of the Central Histaminergic System in Behavioral State Control
Arrigoni, E., & Fuller, P. M. (2021) · Current topics in behavioral neurosciences · doi:10.1007/7854_2021_263 · Cited by 17
The histamine H1 receptor and recollection-based discrimination in a temporal order memory task in the mouse
Zlomuzica, A., Dere, D., & Dere, E. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.08.008 · Cited by 17
“However, therewere also negative reports of normal performance e.g., in the inhibitory avoidance task (Yanai et al., 1998) and object–place recognition task (Zlomuzica et al., 2008) or improved learning and memory performance in a contextual fear-conditioning task (Dai et al., 2007).”
Influential
Regulation of histidine metabolism by Lactobacillus Reuteri mediates the pathogenesis and treatment of ischemic stroke
Hu, K., Zhou, Z., Li, H., Xiao, J., Shen, Y., Ding, K., Zhang, T., Wang, G., Hao, H., & Liang, Y. (2024) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2024.10.003 · Cited by 17
“Previous reports showed that mice lacking HA or HA receptors exhibited cognitive and behavioral impairments 19 .”
Dried bonito broth improves cognitive function via the histaminergic system in mice
Nozawa, Y., Mimura, M., Yamada, K., Sugita, M., Shibakusa, T., & Koyama, N. (2014) · Biomedical Research · doi:10.2220/biomedres.35.311 · Cited by 15
“Blood and hypothalamus were collected from the mice at 15, 30, 45, 60, 90, and 120 min and 60, 120, 240, and 360 min after the adory (1, 8, 9).”
Method
Histamine H3 Receptors and Its Antagonism as a Novel Mechanism for Antipsychotic Effect : A Current Preclinical and Clinical Perspective
Mahmood, D. (2016) · International Journal of Health Sciences · doi:10.12816/0048906 · Cited by 15
“(48-57) Activation of H1 and H2 receptor leads to excitation, whereas H3 receptor activation causes inhibition of histaminergic neurons, thus, H3 receptors play an important role in regulating brain histaminergic neuron.”
Background
Genetic variation and cognitive dysfunction in opioid‐treated patients with cancer
Kurita, G. P., Ekholm, O., Kaasa, S., Klepstad, P., Skorpen, F., & Sjøgren, P. (2016) · Brain and Behavior · doi:10.1002/brb3.471 · Cited by 15
Ameliorating effect of histamine on impairment of cued fear extinction induced by morphine withdrawal in histidine decarboxylase gene knockout mice
Gong, Y.-X., Shou, W., Feng, B., Zhang, W., Wang, H.-J., Ohtsu, H., & Chen, Z. (2010) · Acta Pharmacologica Sinica · doi:10.1038/aps.2010.136 · Cited by 12
Histamine induces KCNQ channel-dependent gamma oscillations in rat hippocampus via activation of the H1 receptor
Andersson, R., Galter, D., Papadia, D., & Fisahn, A. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.03.003 · Cited by 12
“The H1 and H2 receptors are believed to support cognitive functions because mice lacking either of them exhibit cognitive deficits in addition to decreased activity and wakefulness (Dai et al., 2007; Haas et al., 2008).”
Background
Changes in Histaminergic System in Neuropsychiatric Disorders and the Potential Treatment Consequences
Ling, S., & Swaab, D. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210909144930 · Cited by 9
“Histamine facilitates N-methyl-D-aspartate (NMDA) receptor-dependent long-term potentiation (LTP) via H3R receptors during the second postnatal week, but inhibits synaptic plasticity at later developmental stages [49].”
Background
Neuromodulation of Hippocampal Cells and Circuits
Cobb, S., & Lawrence, J. J. (2010) · Springer eBooks · doi:10.1007/978-1-4419-0996-1_7 · Cited by 13
Memory in humans is unaffected by central H1-antagonism, while objectively and subjectively measured sedation is increased
van Ruitenbeek, P., Vermeeren, A., & Riedel, W. J. (2010) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.12.003 · Cited by 11
Cadmium-induced gut dysbiosis precedes the onset of hippocampus-dependent learning and memory deficits in mice
Wang, H., Lim, J. J., Gu, H., Xia, Z., & Cui, J. Y. (2025) · Toxicology · doi:10.1016/j.tox.2025.154265 · Cited by 11
H2 antihistamines: May be useful for combination therapies in cancer?
Mohamad, N. A., Galarza, T. E., & Martín, G. (2024) · Biochemical Pharmacology · doi:10.1016/j.bcp.2024.116164 · Cited by 10
Histamine facilitates GABAergic transmission in the rat entorhinal cortex: Roles of H1and H2receptors, Na+‐permeable cation channels, and inward rectifier K+channels
Cilz, N. I., & Lei, S. (2017) · Hippocampus · doi:10.1002/hipo.22718 · Cited by 10
“, 2009) or H2 (Dai et al., 2007) receptors impairs spatial memory in rodents.”
Background
The role of the central histaminergic receptors in the exercise-induced improvements of the spatial learning and memory in rats
Taati, M., Moghaddasi, M., Esmaeili, M., Pourkhodadad, S., & Nayebzadeh, H. H. (2014) · Brain Research · doi:10.1016/j.brainres.2014.08.065 · Cited by 11
Repeated histamine pretreatment decreased amnesia induced by post-training administration of the drug in a step-down inhibitory avoidance test in mice.
Ahmadi, S., Malekmohamadi, N., & Zarrindast, M. (2010) · PubMed · Cited by 8
Histamine H1 receptors in dentate gyrus-projecting cholinergic neurons of the medial septum suppress contextual fear retrieval in mice
Li, C., Xiao, L., Lin, W., Li, M., Liu, J., Qiu, X., Li, M., Zheng, Y., Xu, C., Wang, Y., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50042-4 · Cited by 7
“…(H 1 R-KO) mice exhibit a pronounced enhancement in auditory and contextual fear conditioning tests when compared to the respective wild-type mice 13 , whereas the consolidation and expression of conditioned fear have been shown to be impaired by peroral treatment of the ﬁ rst-generation…”
BackgroundResult
Histamine Receptors in the Cross-Talk between Periphery and Brain
Lindskog, M. (2017) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyx018 · Cited by 7
“Blocking either the H1 and H2 receptor in the lateral septum decreases anxiety (Chee and Menard, 2013), and both the H1 and H2 receptor knockout mice show enhanced emotional learning but reduced spatial learning (Dai et al., 2007).”
Background
Ameliorative Effect of a Hippocampal Metabotropic Glutamate– Receptor Agonist on Histamine H1 Receptor Antagonist–Induced Memory Deficit in Rats
Masuoka, T., Mikami, A., & Kamei, C. (2010) · Journal of Pharmacological Sciences · doi:10.1254/jphs.10022fp · Cited by 7

Authors: Dai, H., Kaneko, K., Kato, H., Fujii, S., Jing, Y., Xu, A., Sakurai, E., Kato, M., Okamura, N., Kuramasu, A., & Yanai, K.
Affiliations: Tohoku University (JP)
Yamagata University (JP)
Corresponding author: Yanai, Kazuhiko
ORCID: Dai, Hongmei
Kato, Hiroshi
Fujii, Satoshi
Jing, Yuhong
Xu, Ajing
Okamura, Nobuyuki
Kuramasu, Atsuo
Yanai, Kazuhiko
Venue: Neuroscience Research
Publisher: Elsevier BV
Published: 2007-02
Volume: 57
Issue: 2
Pages: 306-313
ISSN: 0168-0102 (ISSN-L)
DOI: 10.1016/j.neures.2006.10.020
OpenAlex: W2047066043
Cited by: 136
References: 50
Citations by year: 2026: 2 · 2025: 5 · 2024: 7 · 2023: 3 · 2022: 5 · 2021: 7 · 2020: 3 · 2019: 3 · 2018: 7 · 2017: 7 · 2016: 10 · 2015: 5 · 2014: 11 · 2013: 12 · 2012: 8
FWCI: 3.24
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Neuroscience Research (publishedVersion)
PubMed (publishedVersion)
Funders: Japan Society for the Promotion of Science
Ministry of Education, Culture, Sports, Science and Technology
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: histamine H1 receptor, histamine H2 receptor, knockout mice, learning and memory, synaptic plasticity, long-term potentiation, hippocampal CA1, object recognition, Barnes maze, fear conditioning, prefrontal cortex, amygdala, cognitive impairment
MeSH terms: Analysis of Variance, Animals, Cognition Disorders, Conditioning, Psychological, Fear, Hippocampus, Neuropsychological Tests, Receptors, Histamine H1, Receptors, Histamine H2, Long-Term Potentiation, Mice, Knockout, Maze Learning, Mice

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Selective cognitive dysfunction in mice lacking histamine H1 and H2 receptors

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