Adolescent exposure to nicotine impairs adult serial pattern learning in rats

Fountain, Stephen B.; Rowan, James D.; Kelley, Brian M.; Willey, Amanda R.; Nolley, Eric P.

doi:10.1007/s00221-008-1346-4

Cited by 41 publications

(59 citation statements)

References 26 publications

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“…Counotte et al (2011) reported persisting changes in the 5-CSRTT after adolescent nicotine, as have Schneider et al (2012). Fountain et al (2008) found persisting effects on serial pattern learning in adults following adolescent nicotine. As noted, these persisting cognitive effects are roughly consistent with findings of persisting changes in mPFC (Bergstrom et al, 2008) and DG (Ehlinger et al, 2012b) morphology after adolescent nicotine, and the electrophysiological changes reported by the Mansvelder group.…”

Section: Cognitionmentioning

confidence: 91%

Adolescent nicotine induces persisting changes in development of neural connectivity

Smith

McDonald

Bergstrom

et al. 2015

Neuroscience & Biobehavioral Reviews

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Section: Cognitionmentioning

confidence: 91%

Adolescent nicotine induces persisting changes in development of neural connectivity

Smith

McDonald

Bergstrom

et al. 2015

Neuroscience & Biobehavioral Reviews

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“…In addition, recent work with a nose poke version of the SMC task has shown that adolescent nicotine exposure causes sex-selective impairments of serial pattern learning in adult rats. Adolescent nicotine causes impairments of acquisition of chunk-boundary elements in male rats and violation elements in female rats, but spares within-chunk element acquisition in both male and female rats (Fountain, Rowan, Kelley, Willey, & Nolley, 2008; Pickens, Rowan, Bevins, & Fountain, 2013). Thus, both behavioral and pharmacological evidence from the SMC task indicate that learning to anticipate chunk-boundary elements, within-chunk elements, and violation elements depends on different underlying cognitive systems and that these dissociable cognitive systems likely depend on dissociable neural systems (Fountain, 2008; Fountain & Rowan, 2000; Fountain et al, 2012).…”

Section: Introductionmentioning

confidence: 98%

Central cholinergic involvement in sequential behavior: Impairments of performance by atropine in a serial multiple choice task for rats

Fountain

Rowan

Wollan

2013

Neurobiology of Learning and Memory

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Two experiments examined whether muscarinic cholinergic systems play a role in rats’ ability to perform well-learned highly-structured serial response patterns, particularly focusing on rats’ performance on pattern elements learned by encoding rules versus by acquisition of stimulus-response (S-R) associations. Rats performed serial patterns of responses in a serial multiple choice task in an 8-lever circular array for hypothalamic brain-stimulation reward. Two experiments examined the effects of atropine, a centrally-acting muscarinic cholinergic receptor antagonist, on rats’ ability to perform pattern elements where responses were controlled by rules versus elements, such as rule-inconsistent “violation elements” and elements following “phrasing cues,” where responses were controlled by associative cues. In Experiment 1, 3-element chunks of both patterns were signaled by pauses that served as phrasing cues before chunk-boundary elements, but one pattern also included a violation element that was inconsistent with pattern structure. Once rats reached a high criterion of performance, the drug challenge was intraperitoneal injection of a single dose of 50 mg/kg atropine sulfate. Atropine impaired performance on elements learned by S-R learning, namely, chunk-boundary elements and the violation element, but had no effect on performance of rule-based within-chunk elements. In Experiment 2, patterns were phrased and unphrased perfect patterns (i.e., without violation elements). To control for peripheral effects of atropine, rats were treated with a series of doses of either centrally-acting atropine or peripherally-acting atropine methyl nitrate (AMN), which does not cross the blood-brain barrier. Once rats reached a high criterion, the drug challenges were on alternate days in the order 50, 25, and 100 mg/kg of either atropine sulfate or AMN. Atropine, but not AMN, impaired performance in the phrased perfect pattern for pattern elements where S-R associations were important for performance, namely, chunk-boundary elements. However, in the structurally more ambiguous unphrased perfect pattern where rats had fewer cues and presumably relied more on S-R associations throughout, atropine impaired performance on all pattern elements. Thus, intact muscarinic cholinergic systems were shown to be necessary for discriminative control previously established by S-R learning, but were not necessary for rule-based serial pattern performance.

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“…Nicotine exposure in adolescence has also been shown to cause cognitive deficits in adults such as decreased attentional performance, impairments of stimulus-response (S-R) learning, and impairments of memory in several behavioral paradigms (Counotte, Spijker, Burgwal, Hogenboom, Schoffelmeer, Vries, Smit, & Pattij, 2009; Fountain, Rowan, Kelley, Willey, & Nolley, 2008; Jacobsen, Krystal, Einar, Westerveld, Frost, & Pugh, 2005; Schochet, Kelley, & Landry, 2004; Slawecki, Thorsell, & Ehlers, 2004; Spaeth, Barnet, Hunt, & Burk, 2010). …”

Section: Introductionmentioning

confidence: 99%

Paradoxical effects of injection stress and nicotine exposure experienced during adolescence on learning in a serial multiple choice (SMC) task in adult female rats

Renaud

Pickens

Fountain

2015

Neurotoxicology and Teratology

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Nicotine exposure in adolescent rats has been shown to cause learning impairments that persist into adulthood long after nicotine exposure has ended. This study was designed to assess the extent to which the effects of adolescent nicotine exposure on learning in adulthood can be accounted for by adolescent injection stress experienced concurrently with adolescent nicotine exposure. Female rats received either 0.033 mg/hr nicotine (expressed as the weight of the free base) or bacteriostatic water vehicle by osmotic pump infusion on postnatal days 25-53 (P25-53). Half of the nicotine-exposed rats and half of the vehicle rats also received twice-daily injection stress consisting of intraperitoneal saline injections on P26-53. Together these procedures produced 4 groups: No Nicotine / No Stress, Nicotine / No Stress, No Nicotine / Stress, and Nicotine / Stress. On P65-99, rats were trained to perform a structurally complex 24-element serial pattern of responses in the serial multiple choice (SMC) task. Four general results were obtained in the current study. First, learning for within-chunk elements was not affected by either adolescent nicotine exposure, consistent with past work (Pickens, Rowan, Bevins, & Fountain, 2013), or adolescent injection stress. Thus, there were no effects of adolescent nicotine exposure or injection stress on adult within-chunk learning typically attributed to rule learning in the SMC task. Second, adolescent injection stress alone (i.e., without concurrent nicotine exposure) caused transient but significant facilitation of adult learning restricted to a single element of the 24-element pattern, namely, the “violation element,” that was the only element of the pattern that was inconsistent with pattern structure. Thus, adolescent injection stress alone facilitated violation element acquisition in adulthood. Third, also consistent with past work (Pickens et al., 2013), adolescent nicotine exposure, in this case both with and without adolescent injection stress, caused a learning impairment in adulthood for the violation element in female rats. Thus, adolescent nicotine impaired adult violation element learning typically attributed to multiple-item learning in the SMC task. Fourth, a paradoxical interaction of injection stress and nicotine exposure in acquisition was observed. In the same female rats in which violation-element learning was impaired by adolescent nicotine exposure, adolescent nicotine experienced without adolescent injection stress produced better learning for chunk-boundary elements in adulthood compared to all other conditions. Thus, adolescent nicotine without concurrent injection stress facilitated adult chunk-boundary element learning typically attributed to concurrent stimulus-response discrimination learning and serial-position learning in the SMC task. To the best of our knowledge, the current study is the first to demonstrate facilitation of adult learning caused by adolescent nicotine exposure.

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Adolescent exposure to nicotine impairs adult serial pattern learning in rats

Cited by 41 publications

References 26 publications

Adolescent nicotine induces persisting changes in development of neural connectivity

Adolescent nicotine induces persisting changes in development of neural connectivity

Central cholinergic involvement in sequential behavior: Impairments of performance by atropine in a serial multiple choice task for rats

Paradoxical effects of injection stress and nicotine exposure experienced during adolescence on learning in a serial multiple choice (SMC) task in adult female rats

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