Cortico-thalamic connectivity is vulnerable to nicotine exposure during early postnatal development through α4/β2/α5 nicotinic acetylcholine receptors
Open accessAbstract
Tobacco smoke exposure during development can result in lasting alterations in sensory processing and attention. This suggests that some constituent of smoke, such as the primary addictive component, nicotine, alters neurodevelopment. Although many effects of developmental nicotine exposure have been identified in humans and animal models, very few mechanistic studies have identified the molecular and anatomical basis for a defined behavioral consequence of developmental exposure. We show in this study that a mouse model of developmental nicotine exposure results in hypersensitive passive avoidance in adulthood. We have used transgenic mice in which β2 subunit containing nicotinic acetylcholine receptors (β2* nAChRs) are expressed exclusively on corticothalamic neurons (β2 tr(CT) mice) to identify the receptor subtypes involved and also to define the circuit level site of action responsible for this persistent, nicotine-induced behavioral phenotype. Further characterization of the native nAChRs expressed in this circuit indicates that both (α4)(2)(β2)(3) and (α4)(2)(β2)(2)α5 nAChR subtypes are present in corticothalamic projections. Consistent with a role for (α4)(2)(β2)(2)α5 nAChRs in mediating the effect of developmental nicotine exposure on adult passive avoidance behavior, constitutive deletion of the α5 nAChR subunit also alters this behavior. A critical period for this developmental consequence of nicotine exposure was defined by limiting exposure to the early post-natal period. Taken together, these studies identify a novel consequence of developmental nicotine exposure in the mouse, define the nAChR subtypes and neural circuit involved in this behavioral change and delimit the neurodevelopmental period critical for vulnerability to a behavioral alteration that persists into adulthood.
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Nicotine administration during the early postnatal period alters performance in the passive avoidance task in normal mice and in mice with expression of β2 nAChRs exclusively in corticothalamic neurons.
“Nicotine administration during this same period alters performance in the passive avoidance task in normal mice as well as in mice with expression of β2 Ã nAChRs exclusively in corticothalamic neurons (Heath et al. 2010)”
From Mechanisms of Nicotine Addiction (2021) · cites this paper as Heath et al. 2010
The Results section reports that nicotine exposure from birth to weaning altered passive avoidance in mice. It also reports altered performance in mice expressing β2-containing nAChRs exclusively in corticothalamic neurons, but those mice received nicotine throughout gestation as well as postnatally; the paper does not establish the effect of postnatal-only exposure in that group (page not available in our copy). (LLM, conf=0.87)
Experimental — accuracy not yet measuredα5/β2 nAChRs on layer 6 cortical glutamatergic projection neurons to the thalamus are essential in maturation of this circuit and for normal adult performance in passive avoidance.
“α5/ β2 Ã nAChRs on layer 6 cortical glutamatergic projection neurons to the thalamus are essential in maturation of this circuit and for normal adult performance in passive avoidance, a somatosensory aversive learning task (King et al. 2003;Heath et al. 2010).”
From Mechanisms of Nicotine Addiction (2021) · cites this paper as Heath et al. 2010
The Discussion (page unavailable) states that corticothalamic neurons must express β2 and α5 subunits for normal passive avoidance performance. It also says the knockout results suggest an α5-mediated current is important for normal circuit maturation, but does not establish that these receptors are essential for maturation. (LLM, conf=0.86)
Experimental — accuracy not yet measuredSignaling through nicotinic acetylcholine receptors is important for establishing critical periods for activity-dependent shaping of visual cortical function and maturation of thalamocortical and corticothalamic glutamatergic synapses.
“In addition, signaling through nAChRs is also important for establishing critical periods for activity-dependent shaping of visual cortical function (Morishita et al., 2010) and maturation of thalamocortical (Aramakis and Metherate, 1998; Aramakis et al., 2000; Hsieh et al., 2002) and corticothalamic (Heath et al., 2010; Horst et al., 2012; King et al., 2003; Picciotto et al., 1995) glutamatergic”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Heath et al., 2010
Developmental nicotine exposure alters processing of somatosensory stimuli in adult mice via α4β2α5 nicotinic acetylcholine receptors expressed in corticothalamic projections.
“We have shown previously that developmental nicotine exposure alters the processing of somatosensory stimuli in adult mice via α4β2α5 nAChRs expressed in corticothalamic projections [27].”
From Impaired auditory discrimination learning following perinatal nicotine exposure or β2 nicotinic acetylcholine receptor subunit deletion (2012) · cites this paper as [27]
The α4β2α5 nicotinic acetylcholine receptor subtype may have a role in refinement of layer VI corticothalamic terminals.
“It has also been suggested that the α4β2α5 nAChR subtype may have a role in the refinement of the layer VI corticothalamic terminals that permit cortical feedback modulation of thalamic activity [27, 28].”
From Impaired auditory discrimination learning following perinatal nicotine exposure or β2 nicotinic acetylcholine receptor subunit deletion (2012) · cites this paper as [27]
Perinatal exposure using this dose and method has minimal impact on birth weight or early postnatal weight gain or maternal care behavior in this strain while affecting sensory processing in adulthood.
“It has also been shown that perinatal exposure using this dose and method of administration has minimal impact on birth weight or early postnatal weight gain or on measures of maternal care behavior in this strain [42] while affecting sensory processing in adulthood [27].”
From Impaired auditory discrimination learning following perinatal nicotine exposure or β2 nicotinic acetylcholine receptor subunit deletion (2012) · cites this paper as [27]
Enhanced learning has been reported in a fear conditioning task and in performance of passive avoidance, while no differences in learning were observed in a 5-choice serial reaction time paradigm.
“Contrary to this hypothesis, enhanced learning has been reported in a fear conditioning task [57] and in performance of passive avoidance [27], while no differences in learning were observed in a 5-choice serial reaction time paradigm [32].”
From Impaired auditory discrimination learning following perinatal nicotine exposure or β2 nicotinic acetylcholine receptor subunit deletion (2012) · cites this paper as [27]
Mice lacking the β2 subunit were unimpaired in an auditory-cued fear conditioning paradigm and showed hypersensitivity to a somatosensory stimulus in passive avoidance.
“For instance, mice lacking the β2 subunit were unimpaired in an auditory-cued fear conditioning paradigm [66] and showed hypersensitivity to a somatosensory stimulus in passive avoidance [27, 28].”
From Impaired auditory discrimination learning following perinatal nicotine exposure or β2 nicotinic acetylcholine receptor subunit deletion (2012) · cites this paper as [27]
Corticothalamic neurons that provide cortical feedback to modulate thalamic sensory input have been implicated in the altered sensory processing observed following developmental exposure to nicotine.
“Corticothalamic neurons that provide cortical feedback to modulate thalamic sensory input have also been implicated in the altered sensory processing observed following developmental exposure to nicotine [27].”
From Impaired auditory discrimination learning following perinatal nicotine exposure or β2 nicotinic acetylcholine receptor subunit deletion (2012) · cites this paper as [27]
The hypersensitive passive avoidance performance behavior exhibited by β2 knockout mice can be normalized by transgenic expression of this subunit exclusively in corticothalamic neurons during development.
“the hypersensitive passive avoidance performance behavior exhibited by β2 knockout mice [33] can be normalized by transgenic expression of this subunit exclusively in corticothalamic neurons during development [27, 28].”
From Impaired auditory discrimination learning following perinatal nicotine exposure or β2 nicotinic acetylcholine receptor subunit deletion (2012) · cites this paper as [27]
β2* nAChRs have an essential role in the maturation of the sensory processing circuitry and are dispensable once this process is completed.
“These data suggest that β2* nAChRs have an essential role in the maturation of the sensory processing circuitry and that it is dispensable once this process is completed [27, 28].”
From Impaired auditory discrimination learning following perinatal nicotine exposure or β2 nicotinic acetylcholine receptor subunit deletion (2012) · cites this paper as [27]
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- Authors
- Heath, C. J., King, S. L., Gotti, C., Marks, M. J., & Picciotto, M. R.
- Affiliations
- Yale University (US)
- University of Sussex (GB)
- University of Milan (IT)
- University of Colorado Boulder (US)
- Corresponding author
- Picciotto, Marina R
- Venue
- Neuropsychopharmacology
- Published
- 2010-08-25
- Volume
- 35
- Issue
- 12
- Pages
- 2324-2338
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC2955839
- OpenAlex
- W2139868719
- Semantic Scholar
- bcf097dcec056a6a1ffbadf1042d629c4057fadc
- Cited by
- 59
- References
- 59
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2023: 3 · 2022: 3 · 2021: 1 · 2020: 3 · 2019: 3 · 2018: 7 · 2017: 1 · 2016: 5 · 2015: 3 · 2014: 6 · 2013: 6 · 2012: 9
- FWCI
- 2.05
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Figshare (submittedVersion)
- Open Research Online (The Open University) (submittedVersion)
- Funders
- Royal Society
- European Commission (202088)
- National Institutes of Health (DA10455, DA00436)
- Medical Research Council (G0802715)
- National Institute on Drug Abuse (K02DA000436, DA 10455, P30DA015663, R01DA003194, R29DA010455, R01DA010455, DA 00436, R37DA014241)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Keywords
- corticothalamic neurons, nicotinic acetylcholine receptors, passive avoidance, hypersensitivity, postnatal development, brain development, transgenic mice, critical period, tobacco smoke
- MeSH terms
- Animals, Animals, Newborn, Avoidance Learning, Cerebral Cortex, Female, Male, Mice, Inbred C57BL, Mice, Transgenic, Neural Pathways, Nicotine, Pregnancy, Prenatal Exposure Delayed Effects, Radioligand Assay, Receptors, Nicotinic, Thalamus, Mice
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