Differential effects of nicotine exposure on the hippocampus across lifespan

Zeid, Dana; Kutlu, Munir Gunes; Gould, Thomas J.

doi:10.2174/1570159x15666170714092436

Cited by 36Nicotinic Acetylcholine Receptors StudySmoking Behavior and CessationMemory and Neural Mechanisms

Differential effects of nicotine exposure on the hippocampus across lifespan

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Zeid, Dana, Kutlu, Munir Gunes, Gould, Thomas J.·2018·Current Neuropharmacology

DOI 10.2174/1570159x15666170714092436PMC PMC6018186

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Abstract

BACKGROUND: Nicotine exposure affects the hippocampus through activation of hippocampal nicotinic acetylcholine receptors (nAChRs), which are present throughout excitatory and inhibitory hippocampal circuitry. The role of cholinergic functioning in the hippocampus varies across developmental stages so that nicotine exposure differentially affects this region depending upon timing of exposure, producing developmentally distinct changes in structure, function, and behavior. METHODS: We synthesize findings across literature in this area to comprehensively review current understanding of the unique effects of nicotine exposure on the hippocampus throughout the lifespan with a focus on hippocampal morphology, cholinergic functioning, and hippocampusdependent learning and memory. CONCLUSIONS: Chronic and acute nicotine exposure differentially affect hippocampus structure, functioning, and related learning and memory in the perinatal period, adolescence, and aging. Age-related differences in sensitivity to nicotine exposure should be considered in the research of nicotine addiction and the development of nicotine addiction treatments.

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The hippocampus, a crucial region for memory and learning, is heavily impacted by the neurotoxic effects of nicotine, resulting in persistent molecular changes and impairments.
“The hippocampus, a crucial region for memory and learning, is heavily impacted by the neurotoxic effects of nicotine, resulting in persistent molecular changes and impairments [73].”
From Nicotine on the developing brain. (2023) · cites this paper as [73]
The ‘Hippocampal morphology’ and ‘Hippocampal plasticity and associated learning and memory’ sections (pages unavailable) describe lasting changes to learning-and-memory mechanisms and persistent impairments after prenatal or adolescent nicotine exposure. The claim omits that age-of-exposure qualification: the paper says adult-exposure deficits can be transient and discusses possible cognitive benefits in some aging populations. (LLM, conf=0.87)
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Morphologic hippocampal asymmetry in male and female rats
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Distribution of Nicotinic Receptors in the Human Hippocampus and Thalamus
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Association between Alcohol Use and Smoking in Adolescent and Young Adult Twins: A Bivariate Genetic Analysis
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Chronic nicotine restores normal Aβ levels and prevents short-term memory and E-LTP impairment in Aβ rat model of Alzheimer's disease
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“In young adult rodents exposed to nicotine during adolescence, dendritic branching in the DG increased in length and complexity [122], while the opposite effect was observed in CA1 [123].”
Background
Nicotine is a neurotoxin in the adolescent brain: critical periods, patterns of exposure, regional selectivity, and dose thresholds for macromolecular alterations
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Human nicotinic receptors—Their role in aging and dementia
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Nicotine enhances morris water maze performance of young and aged rats
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Development of cholinergic markers in mouse forebrain. I. Choline acetyltransferase enzyme activity and acetylcholinesterase histochemistry
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Nicotine activates immature “silent” connections in the developing hippocampus
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Adolescent exposure to nicotine and/or the cannabinoid agonist CP 55,940 induces gender-dependent long-lasting memory impairments and changes in brain nicotinic and CB <sub>1</sub> cannabinoid receptors
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Development of the α7 nicotinic cholinergic receptor in rat hippocampal formation
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Prenatal Nicotine Exposure Alters the Response to Nicotine Administration in Adolescence: Effects on Cholinergic Systems During Exposure and Withdrawal
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Prenatal nicotine alters nicotinic receptor development in the mouse brain
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The dentate gyrus is sexually dimorphic in prepubescent rats: testosterone plays a significant role
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Nicotine Exposure During a Critical Period of Development Leads to Persistent Changes in Nicotinic Acetylcholine Receptors of Adult Rat Brain
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Alterations in hippocampal cholinergic receptors and hippocampal behaviors after early exposure to nicotine
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Nicotine modulation of fear memories and anxiety: Implications for learning and anxiety disorders
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Prenatal choline exposure alters hippocampal responsiveness to cholinergic stimulation in adulthood
Montoya, D. A. C., White, A. M., Williams, C. L., Blusztajn, J. K., Meck, W. H., & Swartzwelder, H. S. (2000) · Developmental Brain Research · doi:10.1016/s0165-3806(00)00075-4 · Cited by 97 · see citing works
Effects of Gestational Nicotine Exposure on Hippocampal Morphology
Roy, T. S., & Sabherwal, U. (1998) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(97)00137-2 · Cited by 95 · see citing works
Caudate nucleus‐dependent navigational strategies are associated with increased use of addictive drugs
Bohbot, V. D., Balso, D. D., Conrad, K., Konishi, K., & Leyton, M. (2013) · Hippocampus · doi:10.1002/hipo.22187 · Cited by 92 · see citing works
Tobacco-induced neurotoxicity of adolescent cognitive development (TINACD): A proposed model for the development of impulsivity in nicotine dependence
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Age-Related Changes in Neuronal Nicotinic Acetylcholine Receptor Subunit α4 Expression Are Modified by Long-Term Nicotine Administration
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Deficits in development of central cholinergic pathways caused by fetal nicotine exposure: Differential effects on choline acetyltransferase activity and [3H]hemicholinium-3 binding
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Nicotine enhances the learning and memory of aged rats
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Immediate and long-term behavioral effects of a single nicotine injection in adolescent and adult rats
Brielmaier, J. M., McDonald, C. G., & Smith, R. F. (2007) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.09.023 · Cited by 90 · see citing works
In Adolescence, Female Rats Are More Sensitive to the Anxiolytic Effect of Nicotine Than Are Male Rats
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Adolescent nicotine administration alters serotonin receptors and cell signaling mediated through adenylyl cyclase
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Visuospatial Memory Deficits Emerging During Nicotine Withdrawal in Adolescents with Prenatal Exposure to Active Maternal Smoking
Jacobsen, L. K., Slotkin, T. A., Westerveld, M., Mencl, W. E., & Pugh, K. R. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300981 · Cited by 81 · see citing works
Alteration of hippocampal cell proliferation in mice lacking the β2 subunit of the neuronal nicotinic acetylcholine receptor
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Developmental effects of acute, chronic, and withdrawal from chronic nicotine on fear conditioning
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Self-citation
Expression of ?5 nicotinic acetylcholine receptor subunit mRNA during hippocampal and cortical development
Winzer‐Serhan, U. H., & Leslie, F. M. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20357 · Cited by 79 · see citing works
Testosterone Depletion in Adult Male Rats Increases Mossy Fiber Transmission, LTP, and Sprouting in Area CA3 of Hippocampus
Skucas, V. A., Duffy, Á., Harte‐Hargrove, L. C., Magagna‐Poveda, A., Radman, T., Chakraborty, G., Schroeder, C. E., MacLusky, N. J., & Scharfman, H. E. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3857-12.2013 · Cited by 78 · see citing works
Age-dependent differences in nicotine reward and withdrawal in female mice
Kota, D., Martin, B. R., & Damaj, M. I. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1117-8 · Cited by 72 · cited 1× · see citing works
“In contrast, studies investigating the rewarding effects of nicotine have reported that acute nicotine administration produced a conditioned place preference in adolescent rats but not in adult rats [152-156], while others found that nicotine induced conditioned place preference at lower doses in adolescents than the…”
Long-lasting teratogenic effects of nicotine on cognition: Gender specificity and role of AMPA receptor function
Vaglenova, J., Parameshwaran, K., Suppiramaniam, V. D., Breese, C. R., Pandiella, N., & Birru, S. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.06.009 · Cited by 72 · see citing works
Genetic variability in nicotinic acetylcholine receptors and nicotine addiction: Converging evidence from human and animal research
Portugal, G. S., & Gould, T. J. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.05.006 · Cited by 71 · see citing works
Long-term changes in fear conditioning and anxiety-like behavior following nicotine exposure in adult versus adolescent rats
SMITH, L., MCDONALD, C., BERGSTROM, H., BRIELMAIER, J., EPPOLITO, A., WHEELER, T., FALCO, A., & SMITH, R. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.07.014 · Cited by 70 · see citing works
Late emerging effects of prenatal and early postnatal nicotine exposure on the cholinergic system and anxiety-like behavior
Eppolito, A. K., Bachus, S. E., McDonald, C. G., Meador-Woodruff, J. H., & Smith, R. F. (2010) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2009.12.009 · Cited by 69 · see citing works
Cellular, molecular, and genetic substrates underlying the impact of nicotine on learning
Gould, T. J., & Leach, P. T. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.08.004 · Cited by 68 · see citing works
Developmental nicotine exposure induced alterations in behavior and glutamate receptor function in hippocampus
Parameshwaran, K., Buabeid, M. A., Karuppagounder, S. S., Uthayathas, S., Thiruchelvam, K., Shonesy, B. C., Dityatev, A. E., Escobar, M. E., Dhanasekaran, M., & Suppiramaniam, V. D. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0805-4 · Cited by 67 · see citing works
Subchronic nicotine exposure in adolescence induces long-term effects on hippocampal and striatal cannabinoid-CB1 and mu-opioid receptors in rats
Marco, E. M., Granstrem, O., Moreno, E., Llorente, R., Adriani, W., Giovanni Laviola, A., & Viveros, M. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2006.11.013 · Cited by 67 · see citing works
Nicotinic receptors in the dorsal and ventral hippocampus differentially modulate contextual fear conditioning
Kenney, J. W., Raybuck, J. D., & Gould, T. J. (2012) · Hippocampus · doi:10.1002/hipo.22003 · Cited by 65 · see citing works
Nicotine exposure during adolescence alters the rules for prefrontal cortical synaptic plasticity during adulthood
Goriounova, N. A., & Mansvelder, H. D. (2012) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2012.00003 · Cited by 65 · see citing works
Presynaptic modulation of acetylcholine, noradrenaline, and serotonin release in the hippocampus of aged rats with various levels of memory impairments
Birthelmer, A., Stemmelin, J., Jackisch, R., & Cassel, J. (2003) · Brain Research Bulletin · doi:10.1016/s0361-9230(03)00042-x · Cited by 60 · see citing works
Acute and chronic nicotine exposure reverse age-related declines in the induction of long-term potentiation in the rat hippocampus
Fujii, S., & Sumikawa, K. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02057-1 · Cited by 58 · see citing works
Effects of nicotine on neurogenesis and plasticity of hippocampal neurons
Shingo, A. S., & Kito, S. (2005) · Journal of Neural Transmission · doi:10.1007/s00702-005-0370-2 · Cited by 57 · see citing works
The duration of nicotine withdrawal-associated deficits in contextual fear conditioning parallels changes in hippocampal high affinity nicotinic acetylcholine receptor upregulation
Gould, T. J., Portugal, G. S., André, J. M., Tadman, M. P., Marks, M. J., Kenney, J. W., Yildirim, E., & Adoff, M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.01.003 · Cited by 56 · cited 1× · see citing works
“In adult rodents, withdrawal from chronic nicotine exposure is associated with deficits in hippocampus-dependent learning tasks; however, these deficits are markedly transient, lasting only a few days [93].”
Background
Maternal exposure of rats to nicotine via infusion during gestation produces neurobehavioral deficits and elevated expression of glial fibrillary acidic protein in the cerebellum and CA1 subfield in the offspring at puberty
Abdel-Rahman, A. A., Dechkovskaia, A. M., Sutton, J. M., Chen, W., Guan, X., Khan, W. A., & Abou-Donia, M. B. (2005) · Toxicology · doi:10.1016/j.tox.2004.12.037 · Cited by 53 · see citing works
Functional characterization of mouse α4β2 nicotinic acetylcholine receptors stably expressed in HEK293T cells
Karadsheh, M. S., Shah, M. S., Tang, X., Macdonald, R. L., & Stitzel, J. A. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02801.x · Cited by 52 · see citing works
Adolescent male Wistar rats are more responsive than adult rats to the conditioned rewarding effects of intravenously administered nicotine in the place conditioning procedure
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Associative Learning, the Hippocampus, and Nicotine Addiction
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Exposure to prenatal nicotine transiently increases neuronal nicotinic receptor subunit α7, α4 and β2 messenger RNAs in the postnatal rat brain
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Chronic nicotine improves working and reference memory performance and reduces hippocampal NGF in aged female rats
French, K. L., Granholm, A., Moore, A., Nelson, M. E., & Bimonte‐Nelson, H. A. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.01.008 · Cited by 46 · see citing works
Evidence for the presence of the tissue-specific transcription factor Pit-1 in lancelet larvae
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The Effects of Nicotine on Learning and Memory
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Conditioned place preference and self-administration induced by nicotine in adolescent and adult rats
Ahsan, H. M., I. de la Peña, J. B., Botanas, C. J., Kim, H. J., Yu, G. Y., & Cheong, J. H. (2014) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2014.056 · Cited by 42 · see citing works
Chronic neonatal nicotine increases anxiety but does not impair cognition in adult rats.
Huang, L. Z., Liu, X., Griffith, W. H., & Winzer‐Serhan, U. H. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.6.1342 · Cited by 42 · see citing works
Acute nicotine delays extinction of contextual fear in mice
Kutlu, M. G., & Gould, T. J. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.031 · Cited by 42 · see citing works
Prenatal Nicotine and Maternal Deprivation Stress De-Regulate the Development of CA1, CA3, and Dentate Gyrus Neurons in Hippocampus of Infant Rats
Wang, H., & Gondré‐Lewis, M. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065517 · Cited by 41 · see citing works
Role of endogenous nicotinic signaling in guiding neuronal development
Liu, Z., Zhang, J., & Berg, D. K. (2007) · Biochemical Pharmacology · doi:10.1016/j.bcp.2007.05.022 · Cited by 40 · see citing works
Postnatal expression of α2 nicotinic acetylcholine receptor subunit mRNA in developing cortex and hippocampus
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Long‐term effects of chronic nicotine on emotional and cognitive behaviors and hippocampus cell morphology in mice: comparisons of adult and adolescent nicotine exposure
Holliday, E. D., Nucero, P., Kutlu, M. G., Oliver, C., Connelly, K. L., Gould, T. J., & Unterwald, E. M. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13398 · Cited by 38 · see citing works
Self-citation
Adolescent nicotine treatment changes the response of acetylcholine systems to subsequent nicotine administration in adulthood
Slotkin, T. A., Bodwell, B. E., Ryde, I. T., & Seidler, F. J. (2008) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2007.12.009 · Cited by 36 · see citing works
Gestational nicotine exposure regulates expression of AMPA and NMDA receptors and their signaling apparatus in developing and adult rat hippocampus
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Nicotine-induced fibroblast growth factor-2 restores the age-related decline of precursor cell proliferation in the subventricular zone of rat brain
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Sex-selective hippocampal alterations after adolescent nicotine administration: Effects on neurospecific proteins
Xu, Z., Seidler, F. J., Tate, C. A., Garcia, S. J., Slikker, W., & Slotkin, T. A. (2003) · Nicotine & Tobacco Research · doi:10.1080/14622200310001615321 · Cited by 31 · see citing works
Adolescent nicotine exposure disrupts context conditioning in adulthood in rats
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Nicotine-induced impairments of spatial cognition and long-term potentiation in adolescent male rats
Han, G., An, L., Yang, B., Leizhen, S. I., & Zhang, T. (2013) · Human & Experimental Toxicology · doi:10.1177/0960327113494902 · Cited by 29 · see citing works
Early postnatal nicotine exposure causes hippocampus-dependent memory impairments in adolescent mice: association with altered nicotinic cholinergic modulation of LTP, but not impaired LTP
Nakauchi, S., Malvaez, M., Su, H., Kleeman, E., Dang, R., Wood, M. A., & Sumikawa, K. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.12.007 · Cited by 27 · see citing works
Hippocampal increased cell death and decreased cell density elicited by nicotine and/or ethanol during adolescence are reversed during drug withdrawal
Oliveira‐da‐Silva, A., Manhães, A. C., Cristina‐Rodrigues, F., Filgueiras, C. C., & Abreu‐Villaça, Y. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.01.060 · Cited by 26 · see citing works
Long term alterations in synaptic physiology, expression of β2 nicotinic receptors and ERK1/2 signaling in the hippocampus of rats with prenatal nicotine exposure
Parameshwaran, K., Buabeid, M. A., Bhattacharya, S., Uthayathas, S., Kariharan, T., Dhanasekaran, M., & Suppiramaniam, V. D. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.07.007 · Cited by 26 · see citing works
Nicotine Exposure during the Third Trimester Equivalent of Human Gestation: Time Course of Effects on the Central Cholinergic System of Rats
Nunes‐Freitas, A. L., Ribeiro‐Carvalho, A., Lima, C. S., Dutra-Tavares, A. C., Manhães, A. C., Lisboa, P. C., OLIVEIRA, E. B. D., de Moura, E. G., Filgueiras, C. C., & Abreu‐Villaça, Y. (2011) · Toxicological Sciences · doi:10.1093/toxsci/kfr147 · Cited by 26 · see citing works
Chronic treatments with tacrine and (−)-nicotine induce different changes of nicotinic and muscarinic acetylcholine receptors in the brain of aged rat
Zhang, X., Tian, J., Svensson, A., Gong, Z., Meyerson, B. J., & Nordberg, A. K. (2002) · Journal of Neural Transmission · doi:10.1007/s007020200030 · Cited by 25 · see citing works
Exposure to Nicotine During Pregnancy and Altered Learning and Memory in the Rat Offspring
Li, J., Bo, L., Zhang, P., Gao, Q., Li, L., Tang, J., Wu, C., Li, D., Xiao, J., Chen, J., et al. (2014) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntu178 · Cited by 25 · see citing works
Increased responsiveness of hippocampal pyramidal neurons to nicotine in aged, learning-impaired rats
Engstrøm, D. A., Bickford, P. C., de la Garza, R., Young, D. A., & Rose, G. M. (1993) · Neurobiology of Aging · doi:10.1016/0197-4580(93)90010-9 · Cited by 23 · see citing works
Chronic Nicotine Administration Impairs Activation of Cyclic AMP-Response Element Binding Protein and Survival of Newborn Cells in the Dentate Gyrus
Wei, Z., Belal, C., Tu, W., Chigurupati, S., Ameli, N. J., Lu, Y., & Chan, S. L. (2011) · Stem Cells and Development · doi:10.1089/scd.2010.0326 · Cited by 23 · see citing works
Neonatal Nicotine Exposure Alters Hippocampal EEG and Event-Related Potentials (ERPs) in Rats
Slawecki, C. J., Thomas, J. D., Riley, E. P., & Ehlers, C. L. (2000) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(99)00258-0 · Cited by 23 · see citing works
Effects of nicotine exposure during prenatal or perinatal period on cell numbers in adult rat hippocampus and cerebellum: A stereology study
Chen, W. A., King, K. A., Lee, R. E., Sedtal, C. S., & Smith, A. M. (2006) · Life Sciences · doi:10.1016/j.lfs.2006.07.019 · Cited by 22 · see citing works
Hippocampus modulates the behaviorally‐sensitizing effects of nicotine in a rat model of novelty‐seeking: Potential role for mossy fibers
Bhatti, A. S., Hall, P., Ma, Z., Tao, R., & Isgor, C. (2007) · Hippocampus · doi:10.1002/hipo.20310 · Cited by 21 · see citing works
Prenatal exposure to nicotine with associated in utero hypoxia decreased fetal brain muscarinic mRNA in the rat
Mao, C., Yuan, X., Cui, Y., Li, H., Lv, J., Feng, X., Liu, Y., Chen, L., & Xu, Z. (2007) · Brain Research · doi:10.1016/j.brainres.2007.10.089 · Cited by 21 · see citing works
Developmental Hippocampal Neuroplasticity in a Model of Nicotine Replacement Therapy during Pregnancy and Breastfeeding
Mahar, I., Bagot, R. C., Davoli, M. A., Miksys, S. L., Tyndale, R. F., Walker, C., Maheu, M., Huang, S., Wong, T. P., & Mechawar, N. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037219 · Cited by 20 · see citing works
Chronic neonatal nicotine exposure increases excitation in the young adult rat hippocampus in a sex-dependent manner
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Authors: Zeid, D., Kutlu, M. G., & Gould, T. J.
Affiliations: Pennsylvania State University (US)
Corresponding author: Gould, Thomas J.
ORCID: Zeid, Dana
Kutlu, Munir Gunes
Gould, Thomas J.
Venue: Current Neuropharmacology
Publisher: Bentham Science Publishers Ltd.
Published: 2018-05-01
Volume: 16
Issue: 4
Pages: 388-402
ISSN: 1570-159X (ISSN-L)
DOI: 10.2174/1570159x15666170714092436
PMC: PMC6018186
OpenAlex: W2739214898
Cited by: 36
References: 188
Citations by year: 2026: 1 · 2025: 6 · 2024: 8 · 2023: 4 · 2022: 5 · 2021: 6 · 2020: 2 · 2019: 2 · 2018: 2
FWCI: 1.07
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: cc-by-nc
Locations: Current Neuropharmacology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Funders: Pennsylvania State University
National Institute on Drug Abuse (U01DA041632, R01DA017949)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: nicotine exposure, hippocampus, nicotinic acetylcholine receptors, cholinergic activity, hippocampal morphology, learning and memory, lifespan development, perinatal nicotine exposure, adolescence, aging, nicotine dependence
MeSH terms: Aging, Animals, Hippocampus, Humans, Nicotine, Nicotinic Agonists

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