Despite relatively short drinking histories, adolescents with a history of binge drinking demonstrated different patterns of brain functioning and somewhat poorer performance during verbal encoding compared with nondrinkers. Binge drinkers recalled 7% fewer word pairs correctly, and nearly half of binge drinkers did not adequately recall the word pair list (10 out of 16 or 63% accuracy) on the first training session, whereas only one nondrinker did not reach this benchmark on the first trial. Although performance differences were only trends, likely because of limited power, they may point to important implications for academic achievement. Binge drinkers in this study reported relatively few problems related to alcohol use, yet their somewhat poorer verbal learning performance is consistent with previous work showing poorer verbal recall among adolescents with alcohol use disorders (Brown et al., 2000
In addition to subtle performance decrements, binge drinkers exhibited reduced BOLD response during novel verbal encoding in a large region spanning occipital cortex and extending into the right parahippocampal gyrus and medial right precuneus. We observed similar patterns of diminished occipital response during spatial working memory among adolescents with alcohol use disorders (Tapert et al., 2004
) as well as adolescents using marijuana heavily (Schweinsburg et al., 2008
). The reduced occipital cortex activation among binge drinkers could indicate less involvement of visual and linguistic processing while learning verbal material.
Hippocampal ROI analyses revealed no significant group difference. Within-group analyses demonstrated that controls evinced significant activation during novel encoding in the left hippocampus and binge drinkers exhibited such activation at the trend level. In addition, binge drinkers demonstrated significantly diminished fMRI response that extended into the parahippocampal gyrus. The hippocampus and surrounding medial temporal lobe structures, including the parahippocampal gyrus, are known for their role in memory (e.g., Squire and Schacter, 2002
) and may be particularly susceptible to alcohol-related damage. Smaller hippocampal volumes have been observed in adolescents with alcohol use disorders (De Bellis et al., 2000
; Medina et al., 2007
; Nagel et al., 2005
). Furthermore, compromised white matter integrity of fibers originating in the left hippocampus has been shown in an overlapping sample of binge-drinking youths (McQueeny et al., 2009
). Given that rodent studies have indicated that adolescents are more sensitive than adults to alcohol-induced hippocampal neurotoxicity (Pyapali et al., 1999
; Slawecki et al., 2001
; White and Swartzwelder, 2004
), intense levels of alcohol exposure during this developmental stage may be particularly detrimental to brain functioning (Pascual et al., 2007
; Tokunaga et al., 2006
). Although subtle, our results are consistent with these findings of hippocampal differences in adolescent alcohol users.
Binge drinkers exhibited increased BOLD response during learning of new word pairs in frontal, parietal, and cingulate regions. Frontal and parietal cortices have been consistently implicated in working memory, and the cingulate may have a role in verbal storage (for review, see Wager and Smith, 2003
). Our previous work has characterized increased bilateral parietal (BA 7) BOLD response during spatial working memory among adolescents with alcohol use disorders, which may indicate greater working memory–related neural effort among drinkers (Tapert et al., 2004
). A similar pattern of increased response in the same bilateral parietal regions (BA 7, 40) was observed among binge drinkers in the present study. Given our previous findings of diminished prefrontal activation in alcohol-dependent young women (Tapert et al., 2001
) and adolescent marijuana users (Schweinsburg et al., 2008
), we initially hypothesized that binge drinkers in the present study would show a similar reduction in prefrontal activation. However, we instead observed an increase in right superior prefrontal fMRI response during verbal learning. An fMRI study of paired associates learning among youths likewise revealed increased right dorsolateral prefrontal activation among those prenatally exposed to alcohol compared with control youths (Sowell et al., 2007
). The authors concluded that youths with prenatal alcohol exposure may compensate for deficient medial temporal lobe function by using frontal lobe memory networks. Coupled with the somewhat reduced hippocampal and parahippocampal response among binge drinkers, the observed over-activation of frontoparietal systems by binge drinkers in the present study may similarly suggest greater reliance on alternate memory systems during verbal learning.
In addition, left hemispheric activation is typically dominant during verbal learning and working memory tasks (e.g., Wager and Smith, 2003
), yet the prefrontal group difference in the present study was localized in the right hemisphere. Using this same task, we have observed increased activation throughout the right hemisphere, including prefrontal cortex, among older adults with genetic risk for developing Alzheimer’s disease (Han et al., 2007
). We suggested that this right hemispheric activation among those at risk for Alzheimer’s may reflect recruitment of bilateral systems to maintain performance. Furthermore, a recent transcranial magnetic stimulation study noted that intact right prefrontal systems are crucial for suppressing task-irrelevant information during high-load verbal working memory (Sandrini et al., 2008
). Thus, increased right prefrontal activation among binge drinkers in the present study could, in part, reflect increased effort to suppress irrelevant information.
White matter abnormalities may, in part, underlie these brain function differences. Our recent study of an overlapping sample identified reduced white matter integrity among binge drinkers in frontal and parietal regions, as well as in projections to the left hippocampus (McQueeny et al., 2009
). Microstructural white matter disruption has been related to cognitive decrements among adult alcoholics (Pfefferbaum and Sullivan, 2002
; Pfefferbaum et al., 2009
). In addition, we observed abnormal prefrontal white matter volumes among adolescents with alcohol use disorders (Medina et al., 2008
). Thus, altered white matter integrity could partially underlie functional aberrations observed in these regions. Multimodal functional connectivity analyses will refine the nature of these relationships.
The results of this study should be considered in light of possible limitations and considerations for future work. Although a sample size of 12 can be sufficient to characterize differences in whole-brain functioning (Desmond and Glover, 2002
), we may have had limited power to detect subtle differences in hippocampal response. Longitudinal investigations will begin to determine whether binge drinkers exhibit preexisting differences that may contribute to these findings, as well as the neurocognitive implications of continued drinking or cessation. Finally, the paired associates task used in this study is relatively easy, with an average accuracy of 78% in binge drinkers. A more difficult task, such as a verbal list learning task, might have greater ecological validity to late-adolescent academic settings that require more challenging memorization.
In sum, adolescents with histories of heavy episodic drinking demonstrated functional differences and marginally poorer performance during verbal learning as compared with demographically similar nondrinkers. The pattern of increased frontoparietal response and somewhat reduced hippocampal activation could indicate greater reliance on working memory and subtle deficits in consolidation among drinkers. These preliminary results suggest the possibility of altered neural processing of novel verbal information that could underlie verbal learning decrements, despite relatively short and problem-free drinking histories.