Separating the effect of reward from corrective feedback during learning in patients with Parkinson’s disease

Cogn Affect Behav Neurosci (2017) 17:678–695 DOI 10.3758/s13415-017-0505-0 Separating the effect of reward from corrective feedback during learning in patients with Parkinson’s disease Michael Freedberg 1,2 & Jonathan Schacherer 3 & Kuan-Hua Chen 4,5 & Ergun Y. Uc 4,6 & Nandakumar S. Narayanan 4,7 & Eliot Hazeltine 3 Published online: 10 April 2017 # Psychonomic Society, Inc. 2017 Abstract Parkinson’s disease (PD) is associated with procedural learning deficits. Nonetheless, studies have demonstrated that reward-related learning is comparable between patients with PD and controls (Bódi et al., Brain, 132(9), 2385–2395, 2009; Frank, Seeberger, & O’Reilly, Science, 306(5703), 1940–1943, 2004; Palminteri et al., Proceedings of the National Academy of Sciences of the United States of America, 106(45), 19179–19184, 2009). However, because these studies do not separate the effect of reward from the effect of practice, it is difficult to determine whether the effect of reward on learning is distinct from the effect of corrective feedback on learning. Thus, it is unknown whether these group differences in learning are due to reward processing or learning in general. Here, we compared the performance of medicated PD patients to demographically matched healthy controls * Michael Freedberg 1 Department of Psychological and Brain Sciences, University of Iowa, E11 Seashore Hall E, Iowa City, IA 52242-1407, USA 2 Present address: Henry M. Jackson Foundation for the Advancement of Military Medicine, 9000 Rockville Pike, 10 Center Drive, Rm 7D49A, Bethesda, MD 20814, USA 3 Department of Psychological and Brain Sciences, University of Iowa, Iowa City, IA 52242, USA 4 Department of Neurology, University of Iowa, Iowa City, IA 52242, USA 5 Present address: Institute of Personality and Social Research, University of California, Berkeley, CA 94720, USA 6 Neurology Service, Veterans Affairs Medical Center, Iowa City, IA 52242, USA 7 Aging Mind, Brain Initiative, Carver College of Medicine, Iowa City 52242, IA, USA (HCs) on a task where the effect of reward can be examined separately from the effect of practice. We found that patients with PD showed significantly less reward-related learning improvements compared to HCs. In addition, stronger learning of rewarded associations over unrewarded associations was significantly correlated with smaller skin-conductance responses for HCs but not PD patients. These results demonstrate that when separating the effect of reward from the effect of corrective feedback, PD patients do not benefit from reward. Keywords Parkinson’s disease . Reward . Incidental learning . Feedback Reward impacts a wide variety of functions, including attention (Anderson, Laurent, & Yantis, 2011; Roper, Vecera, & Vaidya, 2014), cognitive control (van Steenbergen, Band, & Hommel, 2009, 2012), and visual working memory (Gong & Li, 2014). To improve the chances of obtaining a reward in the future, an organism must use reward to guide learning. Indeed, reward can modulate several forms of learning, including declarative (Adcock, Thangavel, Whitfield-Gabrieli, Knutson, & Gabrieli, 2006; Wittmann, Dolan, & Düzel, 2011; Wittmann et al., 2005), probabilistic (Delgado, Miller, Inati, & Phelps, 2005; Galvan et al., 2005), and procedural learning (Abe et al., 2011; Freedberg, Schacherer, & Hazeltine, 2016; Wachter, Lungu, Liu, Willingham, & Ashe, 2009). A wealth of evidence has demonstrated the basal ganglia’s essential role in feedback-related learning (Aron et al., 2004; Ashby, Noble, Filoteo, Waldron, & Ell, 2003; Bellebaum, Koch, Schwarz, & Daum, 2008; Knowlton, Mangels, & Squire, 1996; Palminteri et al., 2011; Poldrack et al., 2001; Shohamy, Myers, Onlaor, & Gluck, 2004; Shohamy, Myers, Grossman, et al., 2004), and reward processing (Apicella, Ljungberg, Scarnati, & Schultz, 1991; Delgado et al., 2005; Cogn Affect Behav Neurosci (2017) 17:678–695 Galvan et al., 2005; McClure, York, & Montague, 2004; Samanez-Larkin et al., 2007; Wachter et al., 2009). Evidence from neuroimaging studies demonstrate activation of the striatum during feedback-dependent learning (Aron et al., 2004; R. A. Poldrack et al., 2001; R. Poldrack, Prabhakaran, Seger, & Gabrieli, 1999), so it is not surprising that patients with Parkinson’s disease (PD) who experience basal ganglia dysfunction as a result of dopamine neuron loss (Agid, 1991; Agid, Javoy-Agid, & Ruberg, 1987; Hornykiewicz, 1966) experience feedback learning deficits (Ashby et al., 2003; Cools, Barker, Sahakian, & Robbins, 2001; Foerde, Race, Verfaellie, & Shohamy, 2013; Knowlton et al., 1996; D. Shohamy, Myers, Onlaor, et al., 2004; Swainson et al., 2000). Interestingly, despite the feedback-learning deficits exhibited by patients with PD, three recent studies have demonstrated that PD patients are able to learn from reward just as well or better than healthy controls (HCs) when taking their usual antiparkinsonian medication (Bódi et al., 2009; Frank et al., 2004; Palminteri et al., 2009). Although these studies demonstrate that patients can learn to select responses that lead to reward just as well or better than healthy controls (HCs), it is unclear whether reward can improve learning in patients with PD beyond simply providing feedback as to whether the response was correct. This issue has not been resolved because, thus far, the reward aspect of feedback has not been dissociated from the information necessary to learn the task. In other words, in studies showing comparable learning between medicated patients with PD and HCs (Bódi et al., 2009; Frank et al., 2004; Palminteri et al., 2009) the reward also served as the task-relevant information needed to perform the task accurately; there was no distinction between informing the participants that responses were correct and rewarding them. For example, Bódi and colleagues (2009) consistently presented B+25^ as feedback when participants correctly categorized a stimulus and presented no feedback when an incorrect response was selected. Thus, because the reward also signaled that the task had been performed correctly, and because a reward condition was not contrasted with one in which feedback was given without reward, it is difficult to tell whether learning from reward was different from learning only from corrective feedback. A second complication with studying the effect of reward on learning in any population is that it can be difficult to tease apart from incentive learning. In other words, in many cases, it is difficult to determine whether reward directly improves learning processes by Bstamping in^ stimulus-response (S-R) associations (such as the dopamine hypothesis of reinforcement; Wise, 2004), or reward enhances motivational processes, which consequently improves S-R binding. Several imaging studies have shown that the striatum responds to rewards (Delgado et al., 2005; Galvan et al., 2005; Wachter et al., 2009); however, only a few studies have attempted to d (...truncated)