Nicotinic modulation of synaptic transmission and plasticity in cortico-limbic circuits

Mansvelder, Huibert D.; Mertz, Marjolijn; Role, Lorna W.

doi:10.1016/j.semcdb.2009.01.007

Cited by 126Nicotinic Acetylcholine Receptors StudyNeuroscience and Neuropharmacology ResearchSmoking Behavior and Cessation

Nicotinic modulation of synaptic transmission and plasticity in cortico-limbic circuits

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Mansvelder, Huibert D., Mertz, Marjolijn, Role, Lorna W.·2009·Seminars in Cell & Developmental Biology

DOI 10.1016/j.semcdb.2009.01.007PMC PMC2742626

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Abstract

Nicotine is the principle addictive agent delivered via cigarette smoking. The addictive activity of nicotine is due to potent interactions with nicotinic acetylcholine receptors (nAChRs) on neurons in the reinforcement and reward circuits of the brain. Beyond its addictive actions, nicotine is thought to have positive effects on performance in working memory and short-term attention-related tasks. The brain areas involved in such behaviors are part of an extensive cortico-limbic network that includes relays between prefrontal cortex (PFC) and cingulate cortex (CC), hippocampus, amygdala, ventral tegmental area (VTA) and the nucleus accumbens (nAcc). Nicotine activates a broad array of nAChRs subtypes that can be targeted to pre- as well as peri- and post-synaptic locations in these areas. Thereby, nicotine not only excites different types of neurons, but it also perturbs baseline neuronal communication, alters synaptic properties and modulates synaptic plasticity. In this review we focus on recent findings on nicotinic modulation of cortical circuits and their targets fields, which show that acute and transient activation of nicotinic receptors in cortico-limbic circuits triggers a series of events that affects cognitive performance in a long lasting manner. Understanding how nicotine induces long-term changes in synapses and alters plasticity in the cortico-limbic circuits is essential to determining how these areas interact in decoding fundamental aspects of cognition and reward.

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ACh release in the amygdala strengthens associations between environmental stimuli and stressful events, potentially contributing to maladaptive learning underlying affective disorders.
“Thus, ACh release in the amygdala is thought to strengthen associations between environmental stimuli and stressful events, potentially contributing to maladaptive learning underlying affective disorders (Mansvelder et al., 2009).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Mansvelder et al., 2009
Cortico-amygdala glutamatergic connections are strongly and persistently potentiated by nAChR stimulation.
“and cortico-amygdala glutamatergic connections are also strongly and persistently potentiated by nAChR stimulation (Mansvelder et al., 2009).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Mansvelder et al., 2009

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Gotti, C., Moretti, M., Clementi, F., Riganti, L., McIntosh, J. M., Collins, A. C., Marks, M. J., & Whiteaker, P. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.011940 · Cited by 133 · see citing works
α5 Subunit Alters Desensitization, Pharmacology, Ca++ Permeability and Ca++ Modulation of Human Neuronal α3 Nicotinic Receptors
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Presynaptic Opioid and Nicotinic Receptor Modulation of Dopamine Overflow in the Nucleus Accumbens
Britt, J. P., & McGehee, D. S. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4275-07.2008 · Cited by 125 · see citing works
Nicotinic Acetylcholine Receptors at Glutamate Synapses Facilitate Long-Term Depression or Potentiation
Ge, S., & Dani, J. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0542-05.2005 · Cited by 125 · see citing works
A critical period for nicotine-induced disruption of synaptic development in rat auditory cortex
Aramakis, V. B., Hsieh, C. Y., Leslie, F. M., & Metherate, R. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06106.2000 · Cited by 120 · see citing works
Role of α7 nicotinic receptors in nicotine dependence and implications for psychiatric illness
Nomikos, G. G., Schilström, B., Hildebrand, B. E., Panagis, G., Grenhoff, J., & Svensson, T. H. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00204-7 · Cited by 115 · see citing works
Electrophysiological Interactions between Striatal Glutamatergic and Dopaminergic Systems
West, A. R., Floresco, S., Charara, A., Rosenkranz, J., & Grace, A. A. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1300.004 · Cited by 114 · see citing works
Allosteric mechanisms in normal and pathological nicotinic acetylcholine receptors
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α7 Receptor-selective agonists and modes of α7 receptor activation
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Characterization of Nicotinic Agonist-Induced [3H]Dopamine Release from Synaptosomes Prepared from Four Mouse Brain Regions
Grady, S. R., Murphy, K. L., Cao, J., Marks, M. J., McIntosh, J. M., & Collins, A. C. (2002) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.301.2.651 · Cited by 110 · see citing works
Developmental Excitation of Corticothalamic Neurons by Nicotinic Acetylcholine Receptors
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Nicotine-induced plasticity during development: modulation of the cholinergic system and long-term consequences for circuits involved in attention and sensory processing
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GABA mechanisms in the pedunculopontine tegmental nucleus influence particular aspects of nicotine self-administration selectively in the rat
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Functional contribution of the α5 subunit to neuronal nicotinic channels expressed by chick sympathetic ganglion neurones
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CNS Localization of Neuronal Nicotinic Receptors
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3H‐nicotine‐ and 125I‐alpha‐bungarotoxin‐labeled nicotinic receptors in the interpeduncular nucleus of rats. II. Effects of habenular deafferentation
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α7 Nicotinic Acetylcholine Receptors Occur at Postsynaptic Densities of AMPA Receptor-Positive and -Negative Excitatory Synapses in Rat Sensory Cortex
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Presynaptic Type III Neuregulin 1 Is Required for Sustained Enhancement of Hippocampal Transmission by Nicotine and for Axonal Targeting of α7 Nicotinic Acetylcholine Receptors
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Heteromeric Complexes of α5 and/or α7 Subunits: Effects of Calcium and Potential Role in Nicotine‐Induced Presynaptic Facilitation
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Differential effects of ciproxifan and nicotine on impulsivity and attention measures in the 5-choice serial reaction time test
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Critical Role of the Prefrontal Cortex in the Regulation of Hippocampus–Accumbens Information Flow
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A Molecular Link between Inward Rectification and Calcium Permeability of Neuronal Nicotinic Acetylcholine α3β4 and α4β2 Receptors
Haghighi, A. P., & Cooper, E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-02-00529.2000 · Cited by 75 · see citing works
Action Potential-Independent and Nicotinic Receptor-Mediated Concerted Release of Multiple Quanta at Hippocampal CA3–Mossy Fiber Synapses
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Cocaine Sensitization: Modulation by Dopamine D2 Receptors
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Presynaptic Type III Neuregulin1-ErbB signaling targets α7 nicotinic acetylcholine receptors to axons
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Nicotinic receptors and hippocampal synaptic plasticity…it’s all in the timing
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Facilitation of Cortico–Amygdala Synapses by Nicotine: Activity-Dependent Modulation of Glutamatergic Transmission
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Calcium Flux Through Predominantly Independent Purinergic ATP and Nicotinic Acetylcholine Receptors
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Chronic nicotine exposure induces a long-lasting and pathway-specific facilitation of LTP in the amygdalaPreprint
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Immunological cross-reactivity between the α-bungarotoxin-binding component from rat brain and nicotinic acetylcholine receptor
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Estimation of both the potency and efficacy of α7 nAChR agonists from single-concentration responses
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Nicotinic cholinergic stimulation promotes survival and reduces motility of cultured rat cerebellar granule cells
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Synaptic mechanisms and cholinergic regulation in auditory cortex
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Ultrastructural Immunolocalization of the α7 nAChR Subunit in Guinea Pig Medial Prefrontal Cortex
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Selective deletion of the α5 subunit differentially affects somatic–dendritic <i>versus</i> axonally targeted nicotinic ACh receptors in mouse
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Nicotinic modulation of thalamocortical neurotransmission
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Involvement of the fimbria fornix in the initiation but not in the expression of methamphetamine-induced sensitization
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Nicotine and Synaptic Plasticity in Prefrontal Cortex
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Altered Prefrontal Cortex‐Nucleus Accumbens Information Processing in a Developmental Animal Model of Schizophrenia
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3 of the 135 references couldn’t be matched to a known paper.

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Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior
Picciotto, M. R., Higley, M. J., & Mineur, Y. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.036 · Cited by 1,404 · see citing works
Neuromodulation of neurons and synapses
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Sex differences in the neural mechanisms mediating addiction: a new synthesis and hypothesis
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Cognitive Effects of Nicotine: Recent Progress
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Nicotinic α7 receptors enhance NMDA cognitive circuits in dorsolateral prefrontal cortex
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Beyond faithful conduction: Short-term dynamics, neuromodulation, and long-term regulation of spike propagation in the axon
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Neuromodulation by acetylcholine: examples from schizophrenia and depression
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Beyond the Channel: Metabotropic Signaling by Nicotinic Receptors
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4 2 Nicotinic Acetylcholine Receptors on Dopaminergic Neurons Mediate Nicotine Reward and Anxiety Relief
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Developmental aspects of the cholinergic system
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The habenulo-interpeduncular pathway in nicotine aversion and withdrawal
Antolin-Fontes, B., Ables, J. L., Görlich, A., & Ibañez-Tallon, I. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.11.019 · Cited by 154 · see citing works
Prefrontal nicotinic receptors control novel social interaction between mice
Avale, M. E., Chabout, J., Pons, S., Serreau, P., De Chaumont, F., Olivo‐Marin, J., Bourgeois, J., Maskos, U., Changeux, J., & Granon, S. (2011) · The FASEB Journal · doi:10.1096/fj.10-178558 · Cited by 114 · see citing works
An essential role of acetylcholine-glutamate synergy at habenular synapses in nicotine dependence
Frahm, S., Antolin-Fontes, B., Görlich, A., Zander, J.-F., Ahnert-Hilger, G., & Ibañez-Tallon, I. (2015) · eLife · doi:10.7554/elife.11396 · Cited by 98 · see citing works
Multiple Nicotinic Acetylcholine Receptor Subtypes in the Mouse Amygdala Regulate Affective Behaviors and Response to Social Stress
Mineur, Y. S., Fote, G. M., Blakeman, S., Cahuzac, E. L. M., Newbold, S. A., & Picciotto, M. R. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.316 · Cited by 90 · see citing works
Effect of Bupropion Treatment on Brain Activation Induced by Cigarette-Related Cues in Smokers
Culbertson, C. S., Bramen, J. E., Cohen, M. S., London, E. D., Olmstead, R. E., Gan, J. J., Costello, M. R., Shulenberger, S., Mandelkern, M. A., & Brody, A. L. (2011) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.193 · Cited by 80 · see citing works
Development of the motivational system during adolescence, and its sensitivity to disruption by nicotine
Counotte, D. S., Smit, A. B., Pattij, T., & Spijker, S. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.05.010 · Cited by 77 · see citing works
Sensorimotor Gating is Associated with CHRNA3 Polymorphisms in Schizophrenia and Healthy Volunteers
Petrovsky, N., Quednow, B. B., Ettinger, U., Schmechtig, A., Mößner, R., Collier, D. A., Kühn, K.-U., Maier, W., Wagner, M., & Kumari, V. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.12 · Cited by 75 · see citing works
Feasibility Assessment of Micro-Electrode Chip Assay as a Method of Detecting Neurotoxicity in vitro
Defranchi, E., Novellino, A., Whelan, M., Vogel, S., Ramı́rez, T., van Ravenzwaay, B., & Landsiedel, R. (2011) · Frontiers in Neuroengineering · doi:10.3389/fneng.2011.00006 · Cited by 70 · see citing works
Cortical excitability in smoking and not smoking individuals with and without nicotine
Grundey, J., Freznosa, S., Klinker, F., Lang, N., Paulus, W., & Nitsche, M. A. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3125-6 · Cited by 65 · see citing works
Acute nicotine increases both impulsive choice and behavioural disinhibition in rats
Kolokotroni, K. Z., Rodgers, R. J., & Harrison, A. A. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2296-2 · Cited by 60 · see citing works
The multiple roles of the α7 nicotinic acetylcholine receptor in modulating glutamatergic systems in the normal and diseased nervous system
Koukouli, F., & Maskos, U. (2015) · Biochemical Pharmacology · doi:10.1016/j.bcp.2015.07.018 · Cited by 61 · see citing works
Low concentrations of nicotine differentially desensitize nicotinic acetylcholine receptors that include α5 or α6 subunits and that mediate synaptosomal neurotransmitter release
Grady, S. R., Wageman, C. R., Patzlaff, N. E., & Marks, M. J. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.12.026 · Cited by 56 · see citing works
MK-801 disrupts and nicotine augments 40 Hz auditory steady state responses in the auditory cortex of the urethane-anesthetized rat
Sivarao, D. V., Frenkel, M. Y., Chen, P., Healy, F. L., Lodge, N. J., & Zaczek, R. C. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.006 · Cited by 55 · see citing works
Pharmacogenetics of Nicotine Addiction: Role of Dopamine
Herman, A. I., DeVito, E. E., Jensen, K. P., & Sofuoglu, M. (2014) · Pharmacogenomics · doi:10.2217/pgs.13.246 · Cited by 54 · see citing works
Nicotinic α4β2 Cholinergic Receptor Influences on Dorsolateral Prefrontal Cortical Neuronal Firing during a Working Memory Task
Sun, Y.-A., Yang, Y., Galvin, V., Yang, S.-T., Arnsten, A., & Wang, M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0364-17.2017 · Cited by 46 · see citing works
Altered short-term plasticity in the prefrontal cortex after early life seizures
Hernan, A. E., Holmes, G. L., Isaev, D., Scott, R. C., & Isaeva, E. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.10.007 · Cited by 49 · see citing works
Nicotine Elicits Prolonged Calcium Signaling along Ventral Hippocampal Axons
Zhong, C., Talmage, D. A., & Role, L. W. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082719 · Cited by 50 · see citing works
The Volitional Nature of Nicotine Exposure Alters Anandamide and Oleoylethanolamide Levels in the Ventral Tegmental Area
Buczynski, M. W., Polis, I. Y., & Parsons, L. H. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.210 · Cited by 49 · see citing works
Diverse strategies targeting α7 homomeric and α6β2* heteromeric nicotinic acetylcholine receptors for smoking cessation
Brunzell, D. H., McIntosh, J. M., & Papke, R. L. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12421 · Cited by 40 · see citing works
Nicotine primes the effect of cocaine on the induction of LTP in the amygdala
Huang, Y.-Y., Kandel, D. B., Kandel, E. R., & Levine, A. A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.03.031 · Cited by 40 · see citing works
Cortical control of VTA function and influence on nicotine reward
Wu, J., Gao, M., Shen, J.-X., Shi, W., Oster, A. M., & Gutkin, B. S. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.07.013 · Cited by 40 · see citing works
Secondhand Smoke Exposure and Low Blood Lead Levels in Association With Attention-Deficit Hyperactivity Disorder and Its Symptom Domain in Children: A Community-Based Case–Control Study
Joo, H., Lim, M.-H., Ha, M., Kwon, H., Yoo, S. J., Choi, K., & Paik, K.-C. (2016) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntw152 · Cited by 40 · see citing works
The involvement of accumbal glycine receptors in the dopamine-elevating effects of addictive drugs
Jönsson, S., Adermark, L., Ericson, M., & Söderpalm, B. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.03.010 · Cited by 37 · see citing works
Activation and Inactivation of Nicotinic Receptnors in the Dorsal Hippocampal Region Restored Negative Effects of Total (TSD) and REM Sleep Deprivation (RSD) on Memory Acquisition, Locomotor Activity and Pain Perception
Javad-Moosavi, B.-Z., Nasehi, M., Vaseghi, S., Jamaldini, S. H., & Zarrindast, M. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.03.006 · Cited by 36 · see citing works
The alpha7-nicotinic receptor contributes to gp120-induced neurotoxicity: implications in HIV-associated neurocognitive disorders
Capó-Vélez, C. M., Morales‐Vargas, B., García-González, A. P., Grajales‐Reyes, J. G., Delgado‐Vélez, M., Madera, B., Báez-Pagán, C. A., Quesada, O., & Lasalde‐Dominicci, J. A. (2018) · Scientific Reports · doi:10.1038/s41598-018-20271-x · Cited by 33 · see citing works
Revisiting nicotine’s role in the ageing brain and cognitive impairment
Majdi, A., Kamari, F., Vafaee, M. S., & Sadigh‐Eteghad, S. (2017) · Reviews in the Neurosciences · doi:10.1515/revneuro-2017-0008 · Cited by 34 · see citing works
The modulatory role of nicotine on cognitive and non-cognitive functions
Zarrindast, M., & Khakpai, F. (2018) · Brain Research · doi:10.1016/j.brainres.2018.12.002 · Cited by 32 · see citing works
Cellular events in nicotine addiction
Penton, R. E., & Lester, R. A. J. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.01.001 · Cited by 32 · see citing works
Neurobiological and Neurophysiological Mechanisms Underlying Nicotine Seeking and Smoking Relapse
Schmidt, H. D., Rupprecht, L. E., & Addy, N. (2018) · Complex Psychiatry · doi:10.1159/000494799 · Cited by 32 · see citing works
Oxidative stress in the brain of cigarette smoke-induced noxiousness: neuroprotective role of Sesbania grandiflora
Ramesh, T., Sureka, C., Bhuvana, S., & Begum, V. H. (2014) · Metabolic Brain Disease · doi:10.1007/s11011-014-9614-4 · Cited by 32 · see citing works
Preclinical Evidence That Activation of Mesolimbic Alpha 6 Subunit Containing Nicotinic Acetylcholine Receptors Supports Nicotine Addiction Phenotype
Brunzell, D. H. (2012) · Nicotine & Tobacco Research · doi:10.1093/ntr/nts089 · Cited by 32 · see citing works
Modulation of auditory deviance detection by acute nicotine is baseline and deviant dependent in healthy nonsmokers: a mismatch negativity study
Knott, V., Impey, D., Philippe, T. J., Smith, D., Choueiry, J., de la Salle, S., & Dort, H. (2014) · Human Psychopharmacology Clinical and Experimental · doi:10.1002/hup.2418 · Cited by 30 · see citing works
Involvement of rat dopaminergic system of nucleus accumbens in nicotine-induced anxiogenic-like behaviors
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Authors: Mansvelder, H. D., Mertz, M., & Role, L. W.
Affiliations: Vrije Universiteit Amsterdam (NL)
State University of New York (US)
Corresponding author: Role, Lorna W.
ORCID: Mansvelder, Huibert D.
Mertz, Marjolijn
Role, Lorna W.
Venue: Seminars in Cell & Developmental Biology
Publisher: Elsevier BV
Published: 2009-06
Volume: 20
Issue: 4
Pages: 432-440
ISSN: 1084-9521 (ISSN-L)
DOI: 10.1016/j.semcdb.2009.01.007
PMC: PMC2742626
OpenAlex: W2101759298
Cited by: 126
References: 135
Citations by year: 2026: 2 · 2025: 6 · 2024: 2 · 2023: 8 · 2022: 2 · 2021: 2 · 2020: 9 · 2019: 3 · 2018: 11 · 2017: 9 · 2016: 5 · 2015: 8 · 2014: 15 · 2013: 10 · 2012: 19
FWCI: 0.87
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Seminars in Cell and Developmental Biology (publishedVersion)
PubMed (publishedVersion)
VU Research Portal (publishedVersion)
PubMed Central (acceptedVersion)
Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Funders: National Institute of Neurological Disorders and Stroke (R01NS022061)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
Keywords: nicotine, nicotinic acetylcholine receptors, corticolimbic circuits, synaptic plasticity, synaptic transmission, prefrontal cortex, cingulate cortex, hippocampus, amygdala, ventral tegmental area, nucleus accumbens, nicotine dependence, working memory, attention, reward systems, cognitive performance
MeSH terms: Animals, Humans, Synaptic Transmission, Neuronal Plasticity, Nicotine, Tobacco Use Disorder

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Nicotinic modulation of synaptic transmission and plasticity in cortico-limbic circuits

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