Abnormalities in the ability to accurately process the value of rewards and affective states are common to many clinical conditions, including schizophrenia, anxiety and affective disorders, and substance abuse. Likewise, many patients suffering from these conditions fail to appropriately direct and maintain attention to important environmental events, while ignoring events that interfere with normal life activities, such as minor fluctuations in their internal states, stress-inducing environmental cues and self-generated events such as thoughts, memories and hallucinations. Thus, understanding basic processes of attention, learning, motivation, and reward is important to understanding the basis of normal and pathological psychological function. Previous research on this project demonstrated important roles for the amygdala central nucleus (CEA) in maintaining and redirecting attention in the context of simple appetitive associative learning. Under conditions of high attentional load, this brain region is critical for sustained, selective action based on previous learning about an array of cues. Furthermore, CEA is essential for enhancing attention to potentially relevant cues when current task expectancies are violated. Recent research implicates CEA in the learning of positive motivational significance (incentive motivation) to cues that predict rewards, and suggests common processes in the allocation of attention to neutral stimuli, cues and rewards. The proposed research will explore relations between CEA's roles in attention, emotion, and reward in food-based associative learning of rats. The amygdala has long been known to be important in emotion, and the proposed research would investigate the relations between its emotional and cognitive functions. A key feature of this research is the examination of the roles of neural prediction and prediction error signals in both incentive/reward learning and the allocation of attention under conditions in which reward is irrelevant or absent. The research will combine behavioral training procedures, cellular mapping of behaviorally-dependent neural activation by assessing expression of intermediate early genes, functional anatomical methods, and disconnection lesions to map circuitry involved in these aspects of attention and reward. The proposed studies will clarify the CEA's roles in the modulation of basal forebrain cholinergic systems and midbrain-striatal dopamine systems in food-based associative learning.

National Institute of Health (NIH)
National Institute of Mental Health (NIMH)
Method to Extend Research in Time (MERIT) Award (R37)
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Neurobiology of Learning and Memory Study Section (LAM)
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Osborn, Bettina D
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Johns Hopkins University
Schools of Arts and Sciences
United States
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Holland, Peter C (2018) Stimulus preexposure speeds or slows subsequent acquisition of associative learning depending on learning test procedures and response measure. Learn Behav 46:134-156
Chang, Stephen E; Smith, Kyle S (2016) An omission procedure reorganizes the microstructure of sign-tracking while preserving incentive salience. Learn Mem 23:151-5
Dailey, Megan J; Moran, Timothy H; Holland, Peter C et al. (2016) The antagonism of ghrelin alters the appetitive response to learned cues associated with food. Behav Brain Res 303:191-200
Schiffino, Felipe L; Holland, Peter C (2016) Consolidation of altered associability information by amygdala central nucleus. Neurobiol Learn Mem 133:204-213
Holland, Peter C; Schiffino, Felipe L (2016) Mini-review: Prediction errors, attention and associative learning. Neurobiol Learn Mem 131:207-15
Holland, Peter C (2016) Effects of amygdala lesions on overexpectation phenomena in food cup approach and autoshaping procedures. Behav Neurosci 130:357-75
Holland, Peter C (2016) Enhancing second-order conditioning with lesions of the basolateral amygdala. Behav Neurosci 130:176-81
Schiffino, Felipe L; Holland, Peter C (2016) Secondary visual cortex is critical to the expression of surprise-induced enhancements in cue associability in rats. Eur J Neurosci 44:1870-7
Asem, Judith S A; Holland, Peter C (2015) Dorsolateral striatum implicated in the acquisition, but not expression, of immediate response learning in rodent submerged T-maze. Neurobiol Learn Mem 123:205-16
Asem, Judith S A; Schiffino, Felipe L; Holland, Peter C (2015) Dorsolateral striatum is critical for the expression of surprise-induced enhancements in cue associability. Eur J Neurosci 42:2203-13

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