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. 2018 May 28:9:367.
doi: 10.3389/fneur.2018.00367. eCollection 2018.

Nicotinic Restoration of Excitatory Neuroplasticity Is Linked to Improved Implicit Motor Learning Skills in Deprived Smokers

Jessica Grundey  1 , Nivethida Thirugnasambandam  1 , Rosa Amu  1 , Walter Paulus  1 , Michael A Nitsche  1   2
Affiliations

Nicotinic Restoration of Excitatory Neuroplasticity Is Linked to Improved Implicit Motor Learning Skills in Deprived Smokers

Jessica Grundey et al. Front Neurol. .

Abstract

Nicotine has been shown to modulate neuroplasticity, cognition, and learning processes in smokers and non-smokers. A possible mechanism for its effect on learning and memory formation is its impact on long-term depression and long-term potentiation (LTP). Nicotine abstinence in smokers is often correlated with impaired cognitive performance. As neuroplasticity is closely connected to learning and memory formation, we aimed to explore the effect of nicotine spray administration in deprived smokers on paired-associative stimulation (PAS25)-induced neuroplasticity and on performance of the serial reaction time task (SRTT), a sequential motor learning paradigm. Deprived smokers (n = 12) under placebo medication displayed reduced excitatory neuroplasticity induced by PAS25. Plasticity was restored by nicotine spray administration. Likewise, SRTT-performance improved after nicotine spray administration compared to placebo administration (n = 19). The results indicate a restitutional effect of nicotine spray in deprived smokers on both: LTP-like neuroplasticity and motor learning. These results present a possible explanation for persistence of nicotine addiction and probability of relapse.

Keywords: cognition; neuroplasticity; nicotine; non-invasive brain stimulation; smokers.

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Figures

Figure 1
Figure 1
Displays original motor-evoked potential (MEP)-recordings of a smoking individual after administration of nicotine spray (baseline) and then directly after the PAS25-protocoll (t0). PAS25 enhances the transcranial magnetic stimulation-induced MEP-amplitudes as measured by the peak to peak amplitude and read off on the y-axis (MEP-values). mV, millivolt; t0, first timepoint after PAS25-protocoll.
Figure 2
Figure 2
(A) Displays the setup of the serial reaction time task (SRTT). On a computer screen (*) the elements of the sequence (abadbcdacbdc) are shown consecutively and appear as dots at a specific position. A dot at the second position of the screen means that the corresponding second button on the pad needs to be pushed [gray filled box with the letter (B)]. The dot at the third position means that the subject has to push the third button (C), etc. (B) shows the specific SRTT-procedure. The procedure consists of 8 blocks. Block 1 and 6 (gray) replay a random order of dots (pseudorandomized sequence). Hereby, the dots are presented equally frequently in each position and never in the same position in two subsequent trials. In blocks 2–5 and 7–8, the same sequence of 12 dot positions is repeated 10 times (white squares). The black line signifies task routine [decrease of reaction time (RT), GMS], the dotted gray line shows the sequence learning curve. The difference between the task routine curve and the sequence learning curve determines the sequence learning effect (RT difference between block 5 and 6, SS).
Figure 3
Figure 3
Shows the experimental setup of the serial reaction time task (SRTT) and the PAS-25 experiment. Subjects received either placebo or nicotine spray (PLC/NIC) in randomized order. After 10 min, the SRTT/PAS-25 protocol started. For the PAS-25 measurements, the MEP-baseline values were determined before and after drug administration, and then again monitored for up to 120 min post intervention. r = random stimuli; s = sequence stimuli; numbers 1–8 refer to the different blocks; MEP, motor-evoked potentials.
Figure 4
Figure 4
Displays the nicotinergic impact on paired associative stimulation (PAS)-induced excitatory neuroplasticity. Shown are graphs with motor-evoked potential (MEP)-standardized values on the y-axis plotted against different time points poststimulation on the x-axis. In smokers under placebo medication, PAS-25 did not enhance MEP amplitudes, while administration of nicotine spray leads to facilitatory after-effects lasting for up to 60 min after plasticity induction. Filled symbols indicate statistically significant deviations from baseline and asterisks indicate significant differences between the placebo medication and nicotine conditions (Student’s t-test, paired, two-tailed, p < 0.05). Abbreviations: BL, baseline; plc, placebo; spray, nicotine spray; error bars, SEM.
Figure 5
Figure 5
(A) Displays serial reaction time task performance after placebo and nicotine spray administration. Depicted are the absolute reaction times (RTs) (and SEs) and error rates (B) (summation) for both conditions. Block 1 and 6 present random stimuli, the remaining blocks contain the repeated sequence. Smokers during nicotine withdrawal under placebo spray administration display slower RTs in all blocks as compared to those in the nicotine spray condition. Abbreviations: ms, milliseconds; plc, placebo; spray, nicotine spray; *, significant differences in RTs between placebo spray and nicotine spray.
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