The Effects Of Post-learning Alcohol Ingestion On Human Motor Memory Consolidation Part 1
Dec 21, 2023
Abstract
The neurochemical mechanisms underlying motor memory consolidation remain largely unknown.
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Based on converging work showing that ethyl alcohol retrogradely enhances declarative memory consolidation, this work tested the hypothesis that post-learning alcohol ingestion would enhance motor memory consolidation.
In a within-subject and fully counterbalanced design, participants (n = 24; 12M; 12F) adapted to a gradually introduced visual deviation and ingested, immediately after adaptation, a placebo (PBO), a medium (MED) or high (HIGH) dose of alcohol. The alcohol doses were bodyweight and gender-controlled to yield peak breath alcohol concentrations of 0.00% in the PBO, 0.05% in the MED, and 0.095% in the HIGH condition.
Retention was evaluated 24 hours later through reach aftereffects when participants were sober. The results revealed that retention levels were neither significantly nor meaningfully different in both the MED and HIGH conditions as compared to PBO (all absolute Cohen's dz values < 0.2; small to negligible effects), indicating that post-learning alcohol ingestion did not alter motor memory consolidation.
Given alcohol's known pharmacological GABAergic agonist and NMDA antagonist properties, one possibility is that these neurochemical mechanisms do not decisively contribute to motor memory consolidation. As converging work demonstrated alcohol's retrograde enhancement of declarative memory, the present results suggest that distinct neurochemical mechanisms underlie declarative and motor memory consolidation.
Elucidating the neurochemical mechanisms underlying the consolidation of different memory systems may yield insights into the effects of over-the-counter drugs on everyday learning and memory and also inform the development of pharmacological interventions seeking to alter human memory consolidation.
1 | INTRODUCTION
Motor memories are known to undergo consolidation (Brashers-Krug et al., 1996), but the neurochemical mechanisms underlying this process remain largely unknown.
At the moment, human evidence indicates that gamma-aminobutyric acid (GABA)ergic activity (Donchin et al., 2002; Floyer-Lea et al., 2006; Kolasinski et al., 2019; Mooney et al., 2021; Shibata et al., 2017; van Vugt et al., 2020) and N-methyl-D-Aspartate (NMDA) receptor activity (Cherry et al., 2014; Günthner et al., 2016; Hadj Tahar et al., 2004; Kuriyama et al., 2011) contribute to motor learning, suggesting they could also contribute to motor memory consolidation.
On the one hand, by recording magnetic resonance spectroscopy (MRS) data, Kolasinski et al. (2019) showed that motor sequence learning reduces GABA concentrations in the primary motor cortex (M1) while van Vugt et al. (2020) showed that M1 GABA concentrations increase during the learning of a novel auditory-motor mapping.
Although conflicting, this evidence indicates that GABAergic activity changes accompany the learning of novel motor behaviors and could thus mechanistically contribute to motor memory consolidation. On the other hand, through pharmacological interventions, Kuriyama et al. (2011) showed that administering D-cycloserine (an NMDA receptor agonist) before learning a sequential finger-tapping task enhanced learning and consolidation while both Cherry et al. (2014) and Günthner et al. (2016) found that the same treatment did not affect a balance and serial reaction time task, respectively.
Overall, based on the above and further conflictual work on sleep-dependent memory consolidation (Feld, Lange, et al., 2013; Feld, Wilhelm, et al., 2013; Gais et al., 2008; Hadj Tahar et al., 2005; Kuriyama et al., 2011; Morgan et al., 2010; Smith & Smith, 2003), it remains unclear whether and how GABA and NMDA receptor-mediated activity mechanistically contribute to motor memory consolidation.
One insightful framework to gain insight into this issue is the Opportunistic Consolidation Theory (OCT) (Mednick et al., 2011). Namely, the OCT posits that enhancing GABAergic inhibition and inhibiting NMDA receptor activity immediately following learning retrogradely enhances memory consolidation by preventing the interfering influences of additional learning (Mednick et al., 2011).
Four decades of human studies investigating the influence of post-learning ethyl alcohol ingestion-a GABAergic agonist and NMDA antagonist pharmacological agent (Abrahao et al., 2017; Grant & Lovinger, 2018)-on declarative memory consolidation directly support the OCT (Bruce et al., 1999; Bruce et al., 1999; Bruce & Pihl, 1997; Carlyle et al., 2017; Doss et al., 2018; Lamberty et al., 1990; Mueller et al., 1983; Parker et al., 1980, 1981; Tyson & Schirmuly, 1994; Weafer et al., 2016).
For instance, seminal work from Parker et al. (1980) showed that post-learning alcohol ingestion enhanced visual and verbal memory consolidation as compared to placebo (Parker et al., 1980).
One year later, Parker et al. (1981) showed that this relationship was dose-dependent; the greater the amount of alcohol ingested following learning, the greater the memory consolidation enhancements (Parker et al., 1981) Interestingly, separate lines of evidence showed that post-learning alcohol ingestion also enhances kinesthetic memory consolidation (Hewitt et al., 1996; Scholey & Fowles, 2002), evaluated as the capacity to proprioceptively trace shapes.
This indicates that alcohol-induced retrograde enhancements of consolidation are not restricted to declarative memories but could also be extended to other memory systems.
Given the well-known effects of alcohol on mammalian brains (Abrahao et al., 2017; Grant & Lovinger, 2018), its use as a pharmacological agent will allow substantiating if GABA and NMDA receptor activity is part of the neurochemical mechanisms underlying motor memory consolidation.
The objective of this work was to test the hypothesis that ingesting alcohol immediately following learning would enhance motor memory consolidation. In a fully within-subject and placebo-controlled design, participants used their dominant hand to undergo gradual visuomotor adaptation and-immediately after- ingested a beverage (see Figure 1).
Namely, participants either ingested a placebo (PBO), a medium (MED), or a high dose (HIGH) dose of alcohol, designed to induce maximal breath alcohol concentrations (BrAC) of 0.00%, 0.05%, and 0.095%, respectively.
To assess consolidation, retention was evaluated through reach aftereffects 24 h later (Hamel et al., 2017; Hamel et al., 2019; Hamel et al., 2021) when participants were sober again. Based on previous work on declarative memories (Carlyle et al., 2017; Parker et al., 1981), it was hypothesized that alcohol would enhance motor memory consolidation in a dose-dependent manner: HIGH would yield greater retention than MED and MED would yield greater retention levels than PBO.
To determine if alcohol retrogradely enhances consolidation by preventing the interfering influence of additional learning (Doss et al., 2018; Mednick et al., 2011; Mueller et al., 1983), participants took part in a second gradual visuomotor adaptation with their non-dominant hand 60 min following complete ingestion of the beverages (see Figure 1).
2 | METHODS
2.1 | Participants
A total of 24 medication-free, non-smoking, and neurologically healthy participants took part in this experiment (gender-controlled experiment; 12 males, 12 females; 23.25 2.45 years old [Mean SD]).
Two participants were self-reported left-handed, while every other participant was self-reported right-handed. All participants were of legal drinking age for alcohol consumption and had a normal or corrected-to-normal vision. Participants reported drinking an average of 2.5 2 standardized alcohol units (13.5 g of ethanol/unit) at an average frequency of 2 1 occasions per month.
They also reported not using cannabis (available legally in Canada) as well as other substances of abuse. Participants were not eligible for the study if they scored above 8 on the Alcohol Use Disorders Identification Test (Bohn et al., 1995; Saunders et al., 1993), indicative of symptoms of alcohol use disorders. Specifically, participants had a total average AUDIT score of 4.7 1.8.
Female participants took an over-the-counter pregnancy test before each experimental visit to ensure non-pregnancy at the moment of testing. Ethics approval was obtained from the local institutional ethics review board (project ID: 2021-4081) and conformed to the Declaration of Helsinki.
2.2 | Apparatus and procedures
This work used a randomized within-subject placebo-controlled design to control for individual differences in subjective (Morean & Corbin, 2010) and physiological responses to alcohol (Brunelle et al., 2007; Mundt et al., 1997), as well as environmental, biological, and genetics individual differences in alcohol metabolism (Wall et al., 2016).
Experimental visits were carried out in pairs; participants took part in an acquisition session (lasting 3 h), followed by a retention session 24 h later. During the acquisition session, participants had to reach visual targets while learning to compensate for a gradually introduced visual deviation (Hamel et al., 2017, 2019; Hamel, Dallaire-Jean, et al., 2021; Hamel, de la Fontaine, et al., 2021).
During the retention session, the persistence of reach aftereffects was evaluated to infer the extent of motor memory consolidation. (Hamel et al., 2017, 2019; Hamel, Dallaire-Jean, et al., 2021; Hamel, de la Fontaine, et al., 2021). The experimental visit pairs differed based on the beverage's content: one pair of experimental visits for each of the PBO, MED, and HIGH conditions.
Participants thus took part in a total of six experimental visits. To minimize carryover effects between experimental visit pairs, condition ordering was fully counterbalanced (Brooks, 2012) and at least 7 days separated each visit pair.
Importantly, every experimental visit occurred at the same time of day to minimize the effects of circadian rhythms on memory consolidation (Hartsock & Spencer, 2020) and alcohol metabolism (Wasielewski & Holloway, 2001). Details of the procedures are provided in Figure 1 and below.
2.2.1 | Dominant hand acquisition (alcohol-free)
The motor task to be learned was a gradual visuomotor adaptation protocol. The present apparatus and single-trial procedures used for every visuomotor adaptation block of the present work are similar to previous work (Hamel, Dallaire-Jean, et al., 2021; Hamel, de la Fontaine, et al., 2021; Hamel, Lepage, & Bernier, et al., 2021).
Briefly, participants performed centre-out reaching movements towards one of five targets located around a circular array (10 cm radius) from the center of the virtual environment. The targets were located in every workspace quadrant at the following angles: 0, 36, 72, 108, 144, 180, 216, 252, 288 and 324. Their order of appearance was pseudorandomized so that every target would appear once every 10-trial cycle.
Participants were instructed to react as fast as possible to an auditory Go Cue, to produce straight movements with minimal online corrections in a target movement time of 300 ms, and to end their movement by landing the cursor within the presented target's boundaries.
A typical trial lasted about 5 s.
The purpose of the dominant hand acquisition was to induce learning and then manipulate memory consolidation through alcohol ingestion (see Figure 1). The motor task to be learned consisted of compensating for a gradually introduced visual deviation (see Figure 1b), which was to prevent participants from gaining awareness of the deviation, therefore allowing them to carry out a fully within-subject learning design (Hamel, Dallaire-Jean, et al., 2021; Hamel, de la Fontaine, et al., 2021; Hamel, Lepage, & Bernier, et al., 2021).
Using a gradual rather than abrupt deviation was also to minimize the possible anterograde interference with the subsequent learning in the non-dominant hand session, as adaptation through a gradually introduced sensorimotor perturbation does not transfer between limbs (Hamel, Lepage, & Bernier, et al., 2021; Malfait & Ostry, 2004; Werner et al., 2019).
Importantly, participants were sober during dominant hand acquisition (see Figures 1 and 2). Verbal reports confirmed that none of the participants perceived the deviation.
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