Conditional Expression in Corticothalamic Efferents Reveals a Developmental Role for Nicotinic Acetylcholine Receptors in Modulation of Passive Avoidance Behavior

King, Sarah L.; Marks, Michael J.; Grady, Sharon R.; Caldarone, Barbara J.; Koren, Andrei O.; Mukhin, Alexey G.; Collins, Allan C.; Picciotto, Marina

doi:10.1523/jneurosci.23-09-03837.2003

Cited by 73 publications

(70 citation statements)

References 45 publications

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“…Even though we cannot rule out subtle effects of nicotine on placental or brain vascular integrity, which may indirectly impair brain development, it seems more likely that the abnormal behavior observed in PNE mice was caused by the pathological activation of acetylcholine nicotinic receptors (AchNR) during early stages of brain development (Slotkin, 1998;Slotkin, 2004). Consistent with this interpretation, a recent study suggests that the normal activation of AchNR located in cortico-thalamic terminals plays a critical role in the development of neural circuits involved in the regulation of normal fear-associated learning (King et al, 2003). In this study, knocking-out the b2 subunit of these receptors in neonatal, but not adult, mice resulted in increased learning of a fear-associated learning task known as passive avoidance.…”

Section: Discussionmentioning

confidence: 99%

Behavioral Teratogenicity Induced by Nonforced Maternal Nicotine Consumption

Paz

Barsness

Martenson

et al. 2006

Neuropsychopharmacol

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Prenatal nicotine exposure (PNE) has been associated with increased prevalence of attention deficit hyperactivity disorder (ADHD), major depressive disorder (MDD) and substance abuse in exposed children and adolescents. Whether these syndromes are caused by nicotine exposure, or genetic and psychosocial adversities associated with maternal smoking is not completely clear. Animal models suggest a direct impact of PNE. However, the fact that nicotine is forcefully administrated in these paradigms raises some questions about the specificity of these findings. Pregnant C57BI/6J mice were allowed to choose drinking saccharin/nicotine solutions or pure water. Controls could choose saccharin solutions or pure water. Offspring were tested in spontaneous locomotion, fear-associated learning (trace conditioning), addictive (conditioned place preference), and depression-like (learned helplessness) behaviors. There was no significant difference in weight or pup number between the prenatal treatment groups. A significant effect of PNE was observed on spontaneous locomotion, preference for a cocaine-associated place, and latency to escape in the learned helplessness paradigm. Surprisingly, PNE mice exhibited an increased learning of trace-conditioned fear-associated cues. The hyperlocomotive behavior reported in animal models of PNE is not likely an artifact of forceful nicotine administration. The increased prevalence of ADHD, MDD and substance abuse observed in PNE children and adolescents is probably caused by direct behavioral teratogenic effects of PNE. The role of PNE as a risk factor of syndromes associated to increased learning of fear-associated cues such as post-traumatic stress disorder (PTSD) warrants further evaluation.

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Section: Discussionmentioning

confidence: 99%

Behavioral Teratogenicity Induced by Nonforced Maternal Nicotine Consumption

Paz

Barsness

Martenson

et al. 2006

Neuropsychopharmacol

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“…Nicotinic currents have also been reported in low-threshold spiking interneurons in layers II/III and V of visual cortex in young rats (Xiang et al, 1998), and of prefrontal cortex in young mice (Couey et al, 2007). It has been shown that knock-out mice deleted for all ␤2-containing nicotinic receptors have deficits in cortically mediated arousal processes (Granon et al, 2003;King et al, 2003;Cohen et al, 2005;Granon and Changeux, 2006). Interestingly, it has been found that the performance of these mice on a behav- ioral task of arousal can be normalized if ␤ 2 subunits are restored in corticothalamic neurons during the first 3 weeks of postnatal development (King et al, 2003).…”

Section: Developmental Changes In Layer VI Nicotinic Receptorsmentioning

confidence: 99%

“…During this time, there is a marked band of high-affinity nicotinic binding in layer VI in the prefrontal cortex (Tribollet et al, 2004), the primary location of corticothalamic neurons. Recent transgenic work shows that nicotinic receptors are expressed by corticothalamic neurons and are present in corticothalamic terminals in mice (King et al, 2003). Nicotinic acetylcholine receptors have been suggested to play a trophic role in the development of cortical neurons and brain circuitry (Belluardo et al, 1999;Brown and Kolb, 2001;Liang et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Developmental Excitation of Corticothalamic Neurons by Nicotinic Acetylcholine Receptors

Kassam¹,

Herman²,

Goodfellow³

et al. 2008

J. Neurosci.

129

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In this study, we show robust nicotinic excitation of pyramidal neurons in layer VI of prefrontal cortex. This layer contains the corticothalamic neurons, which gate thalamic activity and play a critical role in attention. Our experiments tested nicotinic excitation across postnatal development, using whole-cell recordings in prefrontal brain slices from rats. These experiments showed that layer VI neurons have peak nicotinic currents during the first postnatal month, a time period of intensive cortical development in rodents. We demonstrate that these currents are mediated directly by postsynaptic nicotinic receptors and can be suppressed by a competitive antagonist of ␣ 4 ␤ 2 * nicotinic receptors. To record from identified corticothalamic neurons, we performed stereotaxic surgery to label the neurons projecting to medial dorsal thalamus. As hypothesized, recordings from these retrogradely labeled neurons in layer VI showed prominent nicotinic currents. Finally, we examined the effects of the drug nicotine on layer VI neurons and probed for the potential involvement of the accessory subunit, ␣ 5 , in their receptors. A level of nicotine similar to that found in the blood of smokers elicits a stable inward current in layer VI neurons, yet this exposure desensitizes ϳ50% of the subsequent current elicited by acetylcholine. An allosteric modulator of ␣ 4 ␤ 2 ␣ 5 receptors resulted in a 2.5-fold potentiation of submaximal nicotinic currents. This result is consistent with the expression of the relatively rare ␣ 5 nicotinic subunit in layer VI. In summary, we show that layer VI corticothalamic neurons can be strongly excited during development by an unusual subtype of nicotinic receptor.

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“…Nicotine administration during the early postnatal period in the rodent disrupts auditory learning and nicotinic regulation of primary auditory cortex (Hsieh et al, 2002;Liang et al, 2006). High-affinity nAChRs expressed on corticothalamic efferents during development are critical for normal passive avoidance learning (King et al, 2003). Stimulation of nAChRs by nicotine may also alter timing of the switch in action of GABA from excitation to inhibition, which may disrupt circuit development (Liu et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Prenatal and Adolescent Exposure to Tobacco Smoke Modulates the Development of White Matter Microstructure

Jacobsen

Picciotto²,

Heath³

et al. 2007

J. Neurosci.

131

114

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Prenatal exposure to maternal smoking has been linked to cognitive and auditory processing deficits in offspring. Preclinical studies have demonstrated that exposure to nicotine disrupts neurodevelopment during gestation and adolescence, possibly by disrupting the trophic effects of acetylcholine. Given recent clinical and preclinical work suggesting that neurocircuits that support auditory processing may be particularly vulnerable to developmental disruption by nicotine, we examined white matter microstructure in 67 adolescent smokers and nonsmokers with and without prenatal exposure to maternal smoking. The groups did not differ in age, educational attainment, IQ, years of parent education, or symptoms of inattention. Diffusion tensor anisotropy and anatomical magnetic resonance images were acquired, and auditory attention was assessed, in all subjects. Both prenatal exposure and adolescent exposure to tobacco smoke was associated with increased fractional anisotropy (FA) in anterior cortical white matter. Adolescent smoking was also associated with increased FA of regions of the internal capsule that contain auditory thalamocortical and corticofugal fibers. FA of the posterior limb of the left internal capsule was positively correlated with reaction time during performance of an auditory attention task in smokers but not in nonsmokers. Development of anterior cortical and internal capsule fibers may be particularly vulnerable to disruption in cholinergic signaling induced by nicotine in tobacco smoke. Nicotine-induced disruption of the development of auditory corticofugal fibers may interfere with the ability of these fibers to modulate ascending auditory signals, leading to greater noise and reduced efficiency of neurocircuitry that supports auditory processing.

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Conditional Expression in Corticothalamic Efferents Reveals a Developmental Role for Nicotinic Acetylcholine Receptors in Modulation of Passive Avoidance Behavior

Cited by 73 publications

References 45 publications

Behavioral Teratogenicity Induced by Nonforced Maternal Nicotine Consumption

Behavioral Teratogenicity Induced by Nonforced Maternal Nicotine Consumption

Developmental Excitation of Corticothalamic Neurons by Nicotinic Acetylcholine Receptors

Prenatal and Adolescent Exposure to Tobacco Smoke Modulates the Development of White Matter Microstructure

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