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«by Amy Lynn Byrd, Ph.D. B.S. in Psychology, College of Charleston, 2006 M.S. in Clinical Psychology, University of Pittsburgh, 2010 Submitted to the ...»

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As such, aberrant reward/punishment processing could result from abnormalities at one or multiple phases. For example, abnormalities may exist during 1) encoding, defined as the initial processing of a stimulus; 2) acquisition, the process of associative learning that occurs with the repeated pairing of two stimuli or stimuli and response; or 3) extinction, the removal of an expected stimulus (Balsam, Drew, & Gallistel, 2010). A failure to evaluate these mechanisms as nuanced processes drastically limits our understanding of their unique contributions to the etiology of CP. While the majority of research to date has utilized complicated tasks that incorporate multiple phases of processing, the current dissertation takes a bottom-up approach, focusing first on a single phase of processing (i.e., encoding) in an attempt to lay the foundation for a more comprehensive understanding of these complex processes.

Recent advances in neuroscience have the potential to build upon behavioral research by further elucidating these mechanisms. Specifically, researchers have identified neural circuitries associated with reward and punishment processing and have linked specific neural substrates to distinct phases of processing. An overview of these circuitries follows along with a review of emerging neuroimaging studies examining reward/punishment processing in youth with CP.

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Extensive empirical work over the past several decades has identified specific neural circuitries associated with reward and punishment processing and emerging neuroimaging work has helped to refine and enhance our understanding of reward and punishment processing systems in the human brain. While a comprehensive examination of the complex circuitry is beyond the scope of this dissertation, there are various subcortical and cortical regions that have been consistently implicated as significant components of these multifaceted networks including the ventral and dorsal striatum (VS and DS, respectively; Delgado, 2007), the amygdala (LeDoux, 2000;

LeDoux, 2003), the anterior cingulate cortex (ACC; Rogers, et al., 2004), the medial prefrontal cortex (mPFC; Clark, Cool, & Robbins, 2004), and the orbital frontal cortex (OFC; Cardinal, Parkinson, Hall, & Everitt, 2002; O'Doherty, Kringelbach, Rolls, Hornak, & Andrews, 2001). A parsimonious overview of these key nodes will be discussed in terms of three neural systems, mirroring the triadic model (Ernst, et al., 2006): 1) reward/ approach; 2) punishment/avoidance;

and 3) regulatory. Although these circuits are discussed here in isolation, it is important to note that there is considerable overlap between systems as well as extensive functional connections that include both direct and indirect projections (Carmichael & Price, 1995; Fuster, 2001;

McDonald, 1991).

2.5.1 Reward/Approach System Extensive research on the reward system has implicated regions of the basal ganglia, namely the striatum, in addition to higher order cortical areas included within the frontal cortex (discussed below). The striatum is comprised of two anatomically and functionally distinct regions: the

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nucleus accumbens (NAcc), and receives input from a variety of regions including the ventral tegmental area (VTA), a region implicated in the initial detection or encoding of a reward stimulus (Fields, Hjelmstad, Margolis, & Nicola, 2007) and the amygdala, an area associated with the emotional salience of reward (Cardinal, et al., 2002; Groenewegen, Wright, Beijer, & Voorn, 1999). Given these afferent connections, it is not surprising that the NAcc has been shown to play an important role in the anticipation or prediction of reward (Knutson & Cooper,

2005) and affective or hedonistic experiences of receiving reward (Cardinal, et al., 2002;

Knutson & Greer, 2008). The DS contains the caudate and putamen, two areas that have been consistently linked to learning reward-response contingencies (Balleine, Delgado, & Hikosaka, 2007; Packard & Knowlton, 2002). Research has shown these regions to be involved in both the acquisition and extinction phases of learning. Specifically, the DS is engaged in rewardprediction errors or the comparison of actual versus predicted rewards as well as the coding of reward-action associations (Delgado, Stenger, & Fiez, 2004; O'Doherty, et al., 2004). For the purpose of the current dissertation, the NAcc, caudate and putamen comprise one region of interest, though distinctions between the VS and DS are noted.

2.5.2 Punishment/Avoidance System Decades of empirical work have identified the amygdala as central to punishment processing, namely classical (aversive) conditioning (LeDoux, 2000; LeDoux, 2003). The amygdala can be divided into two anatomically and functionally distinct components, including the basolateral complex and the central nucleus (Amaral, Price, Pitkanen, & Carmichael, 1992; Swanson, 2003).

In serial processing models, the basolateral complex is linked to processing sensory and

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stimuli contingencies (LeDoux, 2000; 2003). This area has reciprocal projections with various regions of the prefrontal cortex, facilitating its influence on complex behaviors, as well as extensive connections with the VS and central nucleus (Everitt, Cardinal, Parkinson, & Robbins, 2003; Parkinson, Cardinal, & Everitt, 2000). Propagation of this information to the central nucleus serves to mediate a response through projections to the hypothalamus, midbrain reticular formation and brainstem, areas that are associated with behavioral and autonomic responses (Kapp, Whalen, Supple, & Pascoe, 1992). Although the amygdala is noted for its role in the processing of inherently aversive stimuli, it is also implicated in operant conditioning, particularly with stimulus-reinforcement learning (Balleine & Killcross, 2006). Specifically, the basolateral complex and the central nucleus play important roles in the emotional value of other forms of punishment (e.g., loss of money) and are thus thought to influence motivation (Balleine, et al., 2007; Cardinal, et al., 2002). As such, the current dissertation will examine the role of the amygdala in the initial encoding of punishment cues.





2.5.3 Regulatory System The ACC, mPFC and OFC are noted for their involvement in higher order processing and are extensively enervated by direct and indirect projections from subcortical regions linked to reward (i.e., striatum) and punishment (i.e., amygdala) circuitries (Bechara, Damasio, Damasio, & Lee, 1999; Cardinal, et al., 2002; Rogers, et al., 2004). The ACC has been linked to error monitoring of both reward and punishment, with evidence suggesting that it not only detects and monitors errors but also serves to initiate action in response to error detection via connections with the motor system (Rogers, et al., 2004). The rostral-ventral portions of the ACC in particular have

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connections to the mPFC, OFC and striatum (Carmichael & Price, 1996; Öngür & Price, 2000).

The mPFC is involved in outcome evaluation, pattern detection, and decision making (Clark, et al., 2004) and given extensive connections with the amygdala, is thought to play an integral role in emotional learning (Damasio, 1994). The OFC has also been implicated in outcome evaluation and decision making and functions to shape behavior according to the estimated value of actions associated with reward and punishment contingencies (Cardinal, et al., 2002; O'Doherty, et al., 2001). Medial and lateral regions of the OFC respond to various rewards and punishments, respectively and have been implicated in the representational value or magnitude of reward/punishment (Elliott, Dolan, & Frith, 2000). Thus, OFC, mPFC and ACC play distinct roles in the processing of reward and punishment cues and represent three regions of interest in the current study.

2.5.4 Summary It is important to note that while the aforementioned regions of interest represent a central focus of the current dissertation, activation within these regions should be considered within the context of a broader, interconnected circuitry that incorporates aspects of diverse and relevant processes such as attention, arousal and executive control. It is possible that variation in bloodoxygenation level-dependent (BOLD) response in these ROI may be influenced by input from other areas that are beyond the scope of this dissertation. While striatum, amygdala, ACC, mPFC and OFC were ROIs in the current dissertation, whole-brain analyses were also conducted to explore additional neural circuitry that may be involved in processing of reward and punishment

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While various techniques have been used to examine the underlying neurobiology of reward and punishment processing systems, the focus of the current dissertation is functional magnetic resonance imaging (fMRI) due to its ability to spatially localize neural activation during reward and punishment processing. This technique noninvasively quantifies changes in BOLD response, an assessment of the ratio between oxygenated and deoxygenated blood in the brain that is thought to reflect neural activation. Functional MRI is based on the assumption that increases in neuronal activity in a particular area of the brain lead to increases in cerebral blood flow in the same brain areas. Thus, task-specific changes in neural activity can be identified with good temporal and spatial resolution thereby linking the components of a given task to regions of the brain in order to localize specific functions (Buxton, 2002; Toga & Mazziotta, 2002).

As was evident in the behavioral literature, emerging fMRI research among samples of CP youth use a variety of different paradigms. Taken as a whole, results find CP youth to have altered processing in the aforementioned ROIs relative to control groups. Rubia and colleagues (2009) were the first to provide evidence for OFC dysfunction in 9-16 year old youth with CP.

This study utilized a rewarded continuous performance task to examine differences between responsivity to reward vs. non-reward among youth with early-onset CP, youth with ADHD, and healthy controls. Youth with CP demonstrated less activation in the lateral and medial OFC

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evaluation and the representational value of reward/punishment (Elliott, et al., 2000) these results may be interpreted as evidence of a hyposensitivity to reward. In a second study, youth with CP and ADHD showed reduced activation in the ACC while simultaneously showing increased activation in the DS (Gatzke-Kopp, et al., 2009). In this experiment, youth completed a monetary incentive task during which they were rewarded during every other block of trials (i.e., every 10 trials). Differences in this task appeared to be specific to omission of expected reward, suggesting CP may be linked to a failure to process changes in reward contingencies. Along these lines a recent study found adolescent youth with CP to evidence greater activation in the VS to reward and perhaps somewhat contrary to early work, greater activation in the mPFC relative to healthy controls (Bjork, Chen, Smith, & Hommer, 2010). Increased activation in the VS as well as prefrontal regions to both the anticipation and receipt of reward has been interpreted as support of a hypersensitivity to reward in CP youth. Overall, while results are indicative of aberrant reward processing and in the absence of expected reward, replication of results in this area are limited and somewhat inconsistent.

Two additional studies have attempted to examine reward/punishment processing in subgroups of CP youth between the ages of 10 and 17, focusing on those with increased levels of psychopathic features. Finger and colleagues (2008) examined the BOLD response in CP youth with psychopathic features, youth with ADHD, and healthy controls during a task that requires participants to learn by trial-and-error. CP youth with psychopathic features demonstrated increased activation in the OFC as well as the DS (i.e., caudate) during punished errors, though no differences were seen in responsivity to correct rewarded responses. This increase in activation was also positively associated with a continuous measure of CU traits; CP youth with

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punished errors. This somewhat mirrors findings seen in undifferentiated samples of CP youth, with differences in processing most prominent during trials of absent expected reward (GatzkeKopp, et al., 2009) and at the same time provides some evidence for hypersensitivity to the receipt of reward in CP youth with psychopathic features relative to controls. Somewhat contrary to these findings, a later study by Finger and colleagues (2011) found CP youth with psychopathic features to demonstrate reduced responsivity in the OFC to rewarded trials relative to healthy controls, with no notable differences in response to the absence of expected reward or in response to punished errors. Such results may be interpreted as evidence of a hypo-sensitivity to reward.

2.6.1 Summary Though an examination of the underlying neurobiology has the potential to further elucidate mechanisms subserving behavioral differences, there is a paucity of fMRI studies in youth with CP. Therefore, it is difficult to draw firm conclusions from the limited and inconsistent research in this area. While some studies provide support for a hypo-responsivity to reward in CP youth (e.g., Rubia, et al., 2009), others suggest that youth with CP are hypersensitive to reward (e.g., Bjork, et al., 2010). There is also some indication that CP in youth may be less related to abnormalities in processing reward and more associated with a failure to process contingency change, specifically when it involves a failure to receive an expected reward (e.g., Finger, et al., 2008; Gatzke-Kopp, et al., 2009). Attempts to examine the extent to which aberrant reward/punishment processing may be most pronounced or specific to a subgroup of youth characterized by psychopathic features or CU traits mirrors the inconsistency seen in

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and failed to include a group of CP without CU traits/psychopathic features, limiting conclusions about the specificity of these findings among this subgroup.

In light of the aforementioned limitations, the current dissertation seeks to extend and further clarify past literature by examining potential abnormalities in reward and punishment processing among subgroups of youth with CP between the ages of 8-11 relative to HC.



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