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New Learning of Music After Bilateral Medial Temporal Lobe Damage: Evidence from an Amnesic Patient

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New Learning of Music After Bilateral Medial Temporal Lobe Damage: Evidence from an Amnesic Patient ORIGINAL RESEARCH ARTICLE published: 03 September 2014 HUMAN NEUROSCIENCE doi: 10.3389/fnhum.2014.00694 New learning of music after bilateral medial temporal lobe damage: evidence from an amnesic patient Jussi Valtonen1*, Emma Gregory 2, Barbara Landau 2 and Michael McCloskey 2 1 Institute of Behavioural Sciences, University of Helsinki, Helsinki, Finland 2 Department of Cognitive Science, Johns Hopkins University, Baltimore, MD, USA Edited by: Damage to the hippocampus impairs the ability to acquire new declarative memories, but Isabelle Peretz, Université de not the ability to learn simple motor tasks. An unresolved question is whether hippocampal Montréal, Canada damage affects learning for music performance, which requires motor processes, but in a Reviewed by: cognitively complex context. We studied learning of novel musical pieces by sight-reading Séverine Samson, Université de Lille, France in a newly identified amnesic, LSJ, who was a skilled amateur violist prior to contract- Aline Moussard, Rotman Research ing herpes simplex encephalitis. LSJ has suffered virtually complete destruction of the Institute, Canada hippocampus bilaterally, as well as extensive damage to other medial temporal lobe struc- *Correspondence: tures and the left anterior temporal lobe. Because of LSJ’s rare combination of musical Jussi Valtonen, Institute of Behavioural Sciences, University of training and near-complete hippocampal destruction, her case provides a unique oppor- Helsinki, P.O. Box 9, Helsinki tunity to investigate the role of the hippocampus for complex motor learning processes FI-00014, Finland specifically related to music performance. Three novel pieces of viola music were com- e-mail: jussi.valtonen@helsinki.fi posed and closely matched for factors contributing to a piece’s musical complexity. LSJ practiced playing two of the pieces, one in each of the two sessions during the same day. Relative to a third unpracticed control piece, LSJ showed significant pre- to post-training improvement for the two practiced pieces. Learning effects were observed both with detailed analyses of correctly played notes, and with subjective whole-piece performance evaluations by string instrument players. The learning effects were evident immediately after practice and 14 days later. The observed learning stands in sharp contrast to LSJ’s complete lack of awareness that the same pieces were being presented repeatedly, and to the profound impairments she exhibits in other learning tasks. Although learning in sim- ple motor tasks has been previously observed in amnesic patients, our results demonstrate that non-hippocampal structures can support complex learning of novel musical sequences for music performance. Keywords: music performance, learning, memory, hippocampus, brain damage, anterograde amnesia, single- patient study INTRODUCTION of musically proficient neuropsychological research patients [see Performing music has been described as one of the most demand- Peretz and Zatorre (2005), Zatorre et al. (2007), and Levitin and ing forms of skilled serial action human beings are capable of Tirovolas (2009), for reviews on the cognitive neuroscience of (e.g., Palmer, 1997; Altenmüller and Schneider, 2009). The musi- music]. cian must execute intricate musical sequences expressively under In this article, we address a central question concerning the precise timing constraints, following a hierarchically organized neural bases for music performance, asking whether the hip- rhythmic structure while simultaneously preparing for subsequent pocampus is necessary for learning to perform new musical pieces notes. Behavioral studies have revealed many important aspects of by sight-reading. We studied the learning of novel musical pieces the cognitive mechanisms that support music performance (Slo- by a newly identified amnesic patient, LSJ, who was a skilled boda, 1984, 1985; Palmer and van de Sande, 1993, 1995; Chaffin amateur violist prior to suffering virtually complete bilateral and Imreh, 1997, 2002; Engel et al., 1997; Palmer, 1997, 2005, destruction of her hippocampus due to herpes encephalitis. 2006; Drake and Palmer, 2000; Finney and Palmer, 2003; Palmer The hippocampus, located within the brain’s medial tempo- and Pfordresher, 2003; Stewart, 2005; Brodsky et al., 2008; Chaffin ral lobes (MTL), is crucial for the acquisition of new declarative et al., 2009; Lehmann and Kopiez, 2009; Snyder, 2009; Simmons, memories – memories that can be voluntarily retrieved (Scoville 2012; van Vugt et al., 2012; Verrel et al., 2013). However, relatively and Milner, 1957; Eichenbaum, 2000, 2013; Squire and Knowlton, few studies have shed light on the neural substrates. Among the 2000; Corkin, 2002; Insausti et al., 2013). In contrast, it has been reasons for the relative dearth of cognitive neuroscience research argued that “procedural” or “motor” learning relies on structures on music performance are technical difficulties in neuroimaging other than the hippocampus and surrounding MTL areas (Squire complex motor behavior, a lack of animal models, and the scarcity et al., 2004; Eichenbaum, 2013; Reber, 2013). Consistent with Frontiers in Human Neuroscience www.frontiersin.org September 2014 | Volume 8 | Article 694 | 1 Valtonen et al. Music learning after MTL damage this contention, a number of studies have reported that amnesic Palmer and Pfordresher, 2003; Palmer, 2006). In skilled musicians, patients, including those with severe hippocampal damage, may these mental plans include representations both specific for and show preserved capacities for certain forms of non-declarative independent of the motor programs used to execute them (Slo- learning (Milner, 1962; Corkin, 1968, 2002; Stefanacci et al., 2000; boda, 1984; Palmer and Meyer, 2000; Meyer and Palmer, 2003; Eichenbaum, 2013). These results raise the possibility that learn- Palmer, 2005, 2006; Brodsky et al., 2008). ing to perform new pieces of music may be achievable in the In all likelihood, both hippocampal and non-hippocampal absence of the hippocampus. However, it is not entirely clear that structures normally support the complex processes involved in the forms of learning demonstrated by amnesic patients in prior learning to perform a novel piece. Several lines of indirect evi- studies are comparable in complexity to learning musical pieces dence suggest that the hippocampus is especially important. First, for performance. outside the domain of music, the hippocampus has been shown Learning to perform a piece of music has at times been equated to be important both for the learning of single items and for the with “procedural,” “non-declarative,” or “motor” learning (e.g., ability to form associations between previously unrelated items Crystal et al., 1989; Cowles et al., 2003; Cavaco et al., 2012; (Henke et al., 1999; Eichenbaum, 2000; Stark et al., 2002; O’Kane Simmons, 2012), implying that music performance recruits only et al., 2004; Squire et al., 2004; Schapiro et al., 2014). As musical learning processes for which the hippocampus is not critical. How- pieces are composed from a limited number of basic elements, ever, applying this terminology to music performance may be the ability to form associations between items should be of central misleading. Stanley and Krakauer(2013) have recently argued importance in learning any new piece of music. Second, some have that many motor skills such as music performance involve con- suggested that the hippocampus plays a special role in memory siderable cognitive complexity not required by the simple motor under conditions that require combining information from mul- tasks that define procedural learning. As they point out, the dis- tiple sources (Squire and Knowlton, 2000; Nadel and Peterson, tinction between declarative and procedural (or non-declarative) 2013); music performance requires integrating separate aspects learning was originally based on studies with amnesic patient HM, of musical information related to pitch, rhythm, and meter from who had portions of his hippocampus and surrounding MTL visual, auditory, and tactile sensory modalities. Third, music per- structures surgically removed. HM exhibited wide-ranging and ception studies have shown that damage to the MTL region impairs profound impairments in various learning tasks requiring explicit the ability to learn new melodies in recognition tasks (Wilson and retrieval, but showed improvement through repetition in sim- Saling, 2008), and fMRI studies indicate that the hippocampus is ple motor tasks such as mirror drawing (Milner, 1962; Corkin, recruited in memory tasks involving recognition of novel melodies 1968, 2002; Eichenbaum, 2013). In contrast to how these results (Watanabe et al., 2008). have often been interpreted, Stanley and Krakauer(2013) contend Additional evidence that the hippocampus is important for that what HM acquired in mirror drawing was not a motor skill learning music comes from neuroimaging studies demonstrat- but improved motor acuity, one component of motor skill. HM ing that the hippocampus is engaged when complex temporal gained fine-tuned precision through repetition of explicitly indi- sequences are learned during motor performance. Specifically, cated, identical motor movements. Complex motor skills such as evidence comes from the serial reaction time task (SRT task; music performance require not only motor acuity but also the Nissen and Bullemer, 1987; Janata and Grafton, 2003; Schendan ability to select the correct actions on the basis of factual knowl- et al., 2003),
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