Role of amygdala systems in associative learning

Summary

Principal Investigator: Peter Holland
Abstract: Previous research in this project investigated behavioral and neural bases of two changes in attentional processing in associative learning mediated by the amygdala central nucleus (CN): the potentiation of orienting to conditioned stimuli (CSs) paired with food unconditioned stimuli (USs), and the enhancement of CS associability that occurs when contingencies between the CS and other events are altered. The proposed research extends that work by investigating the relation of these attentional changes to other aspects of attention, and by continuing systems analysis of these functions. The project will use a variety of behavioral procedures, asymmetrical lesion techniques, transient, reversible inactivation procedures, and electrophysiological recording methods, with rat subjects, to address four specific aims. The first aim is to distinguish between CN-systems effects on the acquisition and expression of conditioned orienting and associability changes. The second aim is to examine cortical neural encoding of attentional changes in associative learning that depend on CN and its regulation of the basal forebrain cholinergic system. The third aim is to examine the roles of CN attentional systems in performance of selective attention tasks. The fourth aim is to examine cortical activity during performance of selective attention tasks. This research may provide a basis for new insights into cognitive functions of the amygdala, as well as the integration of cognitive and emotional function. In addition, it may have wide clinical implications, because the neural systems to be studied are involved in a number of pathological conditions, for example, Alzheimer's disease (learning and attention deficits often signal the onset of more complete dementia), schizophrenia (deficits in focusing attention on relevant events and ignoring extraneous events), and various affective disorders (inappropriate assignment of motivational value to life events).
Funding Period: 1995-08-01 - 2007-04-19
more information: NIH RePORT

Top Publications

  1. pmc Role of amygdala central nucleus in the potentiation of consuming and instrumental lever-pressing for sucrose by cues for the presentation or interruption of sucrose delivery in rats
    Peter C Holland
    Department of Psychological and Brain Sciences
    Behav Neurosci 128:71-82. 2014
  2. pmc The basolateral amygdala mediates the effects of cues associated with meal interruption on feeding behavior
    Ezequiel M Galarce
    Johns Hopkins University, USA
    Brain Res 1350:112-22. 2010
  3. pmc Assessing the role of the growth hormone secretagogue receptor in motivational learning and food intake
    Alexander W Johnson
    Neurogenetics and Behavior Center, Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, 21218, USA
    Behav Neurosci 123:1058-65. 2009
  4. pmc Role of amygdala central nucleus in aversive learning produced by shock or by unexpected omission of food
    Robert J Purgert
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218, USA
    J Neurosci 32:2461-72. 2012
  5. pmc The effects of basolateral amygdala lesions on unblocking
    Stephen E Chang
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, USA
    Behav Neurosci 126:279-89. 2012
  6. pmc Role of amygdala central nucleus in feature negative discriminations
    Peter C Holland
    Department of Psychological and Brain Sciences, Johns Hopkins University, USA
    Behav Neurosci 126:670-80. 2012
  7. pmc Effects of ventral striatal lesions on first- and second-order appetitive conditioning
    Michael A McDannald
    National Institute on Drug Abuse Intramural Research Program, Baltimore, MD, USA
    Eur J Neurosci 38:2589-99. 2013
  8. pmc Effects of nucleus accumbens core and shell lesions on autoshaped lever-pressing
    Stephen E Chang
    Johns Hopkins University, Baltimore, USA Electronic address
    Behav Brain Res 256:36-42. 2013
  9. pmc Posterior parietal cortex is critical for the encoding, consolidation, and retrieval of a memory that guides attention for learning
    Felipe L Schiffino
    Department of Psychological and Brain Sciences, Johns Hopkins University, 232 Ames Hall, 3400 North Charles Street, Baltimore, MD, 21218, USA
    Eur J Neurosci 39:640-9. 2014
  10. pmc Neural correlates of variations in event processing during learning in basolateral amygdala
    Matthew R Roesch
    Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, Maryland 21201, USA
    J Neurosci 30:2464-71. 2010

Scientific Experts

Detail Information

Publications35

  1. pmc Role of amygdala central nucleus in the potentiation of consuming and instrumental lever-pressing for sucrose by cues for the presentation or interruption of sucrose delivery in rats
    Peter C Holland
    Department of Psychological and Brain Sciences
    Behav Neurosci 128:71-82. 2014
    ..Nevertheless, as in previous studies, CeA was critical to the ability of a CS to enhance instrumental responding. Implications for understanding the nature and basis for incentive learning are discussed...
  2. pmc The basolateral amygdala mediates the effects of cues associated with meal interruption on feeding behavior
    Ezequiel M Galarce
    Johns Hopkins University, USA
    Brain Res 1350:112-22. 2010
    ..These studies extend our knowledge of the psychological and neural processes underlying cue-induced feeding. Understanding these mechanisms may contribute our understanding of the etiology and treatment of binge eating disorders...
  3. pmc Assessing the role of the growth hormone secretagogue receptor in motivational learning and food intake
    Alexander W Johnson
    Neurogenetics and Behavior Center, Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, 21218, USA
    Behav Neurosci 123:1058-65. 2009
    ..These results suggest dissociable functions of GHS-R in its influence over motivational learning and ingestive behavior...
  4. pmc Role of amygdala central nucleus in aversive learning produced by shock or by unexpected omission of food
    Robert J Purgert
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218, USA
    J Neurosci 32:2461-72. 2012
    ..Thus, under these test conditions, different subsets of CeA neurons represented these two aversive states...
  5. pmc The effects of basolateral amygdala lesions on unblocking
    Stephen E Chang
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, USA
    Behav Neurosci 126:279-89. 2012
    ..These results were discussed in the context of roles of the basolateral amygdala in coding and using reward prediction error information in associative learning...
  6. pmc Role of amygdala central nucleus in feature negative discriminations
    Peter C Holland
    Department of Psychological and Brain Sciences, Johns Hopkins University, USA
    Behav Neurosci 126:670-80. 2012
    ..The results are consistent with modern reformulations of both cue and reward processing theories that assign roles for both individual and aggregate error terms in associative learning...
  7. pmc Effects of ventral striatal lesions on first- and second-order appetitive conditioning
    Michael A McDannald
    National Institute on Drug Abuse Intramural Research Program, Baltimore, MD, USA
    Eur J Neurosci 38:2589-99. 2013
    ....
  8. pmc Effects of nucleus accumbens core and shell lesions on autoshaped lever-pressing
    Stephen E Chang
    Johns Hopkins University, Baltimore, USA Electronic address
    Behav Brain Res 256:36-42. 2013
    ..2000a,b), suggesting that the neural circuitry involved in assigning incentive value depends upon the nature of the CS. ..
  9. pmc Posterior parietal cortex is critical for the encoding, consolidation, and retrieval of a memory that guides attention for learning
    Felipe L Schiffino
    Department of Psychological and Brain Sciences, Johns Hopkins University, 232 Ames Hall, 3400 North Charles Street, Baltimore, MD, 21218, USA
    Eur J Neurosci 39:640-9. 2014
    ..We discuss these new results in the context of our previous findings and additional plausible frontoparietal and subcortical networks...
  10. pmc Neural correlates of variations in event processing during learning in basolateral amygdala
    Matthew R Roesch
    Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, Maryland 21201, USA
    J Neurosci 30:2464-71. 2010
    ..These results suggest that basolateral amygdala serves a critical function in attention for learning...
  11. pmc How do you (estimate you will) like them apples? Integration as a defining trait of orbitofrontal function
    Geoffrey Schoenbaum
    Department of Anatomy and Neurobiology, University of Maryland School of Medicine, 20 Penn Street, HSF 2 S251, Baltimore, MD 21201, USA
    Curr Opin Neurobiol 20:205-11. 2010
    ....
  12. pmc Contributions of the amygdala central nucleus and ventrolateral periaqueductal grey to freezing and instrumental suppression in Pavlovian fear conditioning
    Michael A McDannald
    The Johns Hopkins University, 3400 North Charles, 126 Ames Hall, Baltimore, MD 21217, USA
    Behav Brain Res 211:111-7. 2010
    ..These results suggest that the CeA and vlPAG are critically important to expressing fear through conditioned freezing but play different and less critical roles in expressing fear through conditioned suppression...
  13. pmc All that glitters ... dissociating attention and outcome expectancy from prediction errors signals
    Matthew R Roesch
    Department of Psychology, Program in Neuroscience and Cognitive Science, University of Maryland at College Park, College Park, Maryland, USA
    J Neurophysiol 104:587-95. 2010
    ..These results have important implications for how these areas interact to facilitate learning and guide behavior...
  14. pmc Measuring Pavlovian fear with conditioned freezing and conditioned suppression reveals different roles for the basolateral amygdala
    Michael A McDannald
    The Johns Hopkins University, 3400 North Charles, 126 Ames Hall, Baltimore, MD 21217, USA
    Brain Res 1374:82-9. 2011
    ..These findings suggest a critical role for the BLA in fear when assessed with conditioned freezing but a diminished role when assessed with conditioned suppression...
  15. pmc Effects of reward timing information on cue associability are mediated by amygdala central nucleus
    Daniel S Wheeler
    Department of Psychological and Brain Sciences, Johns Hopkins University, 3400 N Charles St, Baltimore, MD 21218, USA
    Behav Neurosci 125:46-53. 2011
    ..These results indicate that the role of CeA in the modulation of associability is not limited to cases of event omission. (PsycINFO Database Record (c) 2011 APA, all rights reserved)...
  16. pmc Interactions between amygdala central nucleus and the ventral tegmental area in the acquisition of conditioned cue-directed behavior in rats
    Hongjoo J Lee
    Department of Psychology, University of Texas, Austin, TX, USA
    Eur J Neurosci 33:1876-84. 2011
    ..The results suggested an excitatory influence of VTA on CeA in the presence of food cues. Implications of these results for brain circuits involved in learned orienting and incentive motivation are discussed...
  17. pmc Effects of cues associated with meal interruption on feeding behavior
    Ezequiel M Galarce
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD 21218, United States
    Appetite 52:693-702. 2009
    ..These experiments may provide a novel animal model of binge-like behaviors in sated rats induced by external cues paired with meal interruption...
  18. pmc The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses
    Thomas C Jhou
    Behavioral Neuroscience Branch, National Institute on Drug Abuse, Baltimore, MD 21224, USA
    Neuron 61:786-800. 2009
    ..These findings suggest that aversive inputs from widespread brain regions and stimulus modalities converge onto the RMTg, which opposes reward and motor-activating functions of midbrain dopamine neurons...
  19. pmc Cognitive versus stimulus-response theories of learning
    Peter C Holland
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218, USA
    Learn Behav 36:227-41. 2008
    ..In the course of describing Spence's views and my research, I hope to communicate some of the richness of Spence's S-R psychology and its currency within modern scientific analyses of behavior...
  20. pmc Amygdala central nucleus function is necessary for learning, but not expression, of conditioned auditory orienting
    Frank Groshek
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD 21218, USA
    Behav Neurosci 119:202-12. 2005
    ..Thus, although the central nucleus is critical to the acquisition of information required for conditioned orienting to auditory cues, it is not needed for maintaining this information for later use...
  21. pmc Orbitofrontal lesions impair use of cue-outcome associations in a devaluation task
    Charles L Pickens
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD 21218, USA
    Behav Neurosci 119:317-22. 2005
    ..Gallagher, P. C. Holland, & G. Schoenbaum, 2003), these results indicate that the OFC is critical for the maintenance of information about the current incentive value of reinforcers or the use of that information to guide behavior...
  22. pmc Role of amygdalo-nigral circuitry in conditioning of a visual stimulus paired with food
    Hongjoo J Lee
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218, USA
    J Neurosci 25:3881-8. 2005
    ..These experiments demonstrate a role for amygdalo-nigral circuitry in learned modulation of attention to signals for biologically significant events...
  23. pmc Variations in unconditioned stimulus processing in unblocking
    Peter C Holland
    Department of Psychological and Brain Sciences, Duke University, Durham, NC, USA
    J Exp Psychol Anim Behav Process 31:155-71. 2005
    ..The roles of reinforcement error signals in conditioning are discussed...
  24. pmc Lesions of orbitofrontal cortex impair rats' differential outcome expectancy learning but not conditioned stimulus-potentiated feeding
    Michael A McDannald
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218, USA
    J Neurosci 25:4626-32. 2005
    ....
  25. ncbi Enhanced conditioning produced by surprising increases in reinforcer value are unaffected by lesions of the amygdala central nucleus
    Peter C Holland
    Johns Hopkins University, USA
    Neurobiol Learn Mem 85:30-5. 2006
    ..These results indicate that CN circuitry implicated in surprise-induced increases in event processing is preferentially engaged when expected events are omitted, and not when unexpected events are presented...
  26. pmc A neural systems analysis of the potentiation of feeding by conditioned stimuli
    Peter C Holland
    Johns Hopkins University, 222 Ames Hall, 3400 North Charles St, Baltimore, MD 21218, USA
    Physiol Behav 86:747-61. 2005
    ....
  27. ncbi Different roles for amygdala central nucleus and substantia innominata in the surprise-induced enhancement of learning
    Peter C Holland
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218, USA
    J Neurosci 26:3791-7. 2006
    ..Additional circuitry linking these brain regions may also be important in the maintenance of that information...
  28. ncbi Role of substantia nigra-amygdala connections in surprise-induced enhancement of attention
    Hongjoo J Lee
    Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218, USA
    J Neurosci 26:6077-81. 2006
    ..These results show that SNc-CeA communication is critical to mechanisms by which the coding of prediction error by midbrain dopamine neurons is translated into enhancement of attention and learning modulated by the cholinergic system...
  29. ncbi Substantia nigra pars compacta is critical to both the acquisition and expression of learned orienting of rats
    Heather El-Amamy
    Johns Hopkins University, 222 Ames Hall, 3400 North Charles Street, Baltimore, MD 21218, USA
    Eur J Neurosci 24:270-6. 2006
    ..Together with our previous findings, these results suggest that the SNc is trained by the CeA during learning and maintains acquired information so that it may modulate DLS sensory-motor function at the time of action...
  30. pmc Reinforcer-specificity of appetitive and consummatory behavior of rats after Pavlovian conditioning with food reinforcers
    Ezequiel M Galarce
    Department of Psychological and Brain Sciences, Johns Hopkins University, 3400 North Charles Street, Baltimore, MD 21218, United States
    Physiol Behav 91:95-105. 2007
    ..The closer an action comes to ingestion, the more it is controlled by sensory properties conveyed by learned cues. These data are discussed in the context of allostatic regulation of food foraging and intake...
  31. pmc Dissociable effects of disconnecting amygdala central nucleus from the ventral tegmental area or substantia nigra on learned orienting and incentive motivation
    Heather El-Amamy
    Johns Hopkins University, Department of Psychological and Brain Sciences, 3400 North Charles Street, Baltimore, MD 21218, USA
    Eur J Neurosci 25:1557-67. 2007
    ..Otherwise, unilateral lesions of either midbrain region impaired transfer. Implications of these results for circuit models of amygdalo-striatal interactions in associative learning are discussed...
  32. pmc Control of appetitive and aversive taste-reactivity responses by an auditory conditioned stimulus in a devaluation task: a FOS and behavioral analysis
    Erin C Kerfoot
    Johns Hopkins University, Baltimore, Maryland 21218, USA
    Learn Mem 14:581-9. 2007
    ..Thus, through associative learning, auditory cues for food gained access to neural processing in several brain regions importantly involved in the processing of taste memory information...
  33. pmc A limited role for mediodorsal thalamus in devaluation tasks
    Charles L Pickens
    Department of Psychological and Brain Sciences, Johns Hopkins University, USA
    Behav Neurosci 122:659-76. 2008
    ....
  34. pmc Temporally limited role of substantia nigra-central amygdala connections in surprise-induced enhancement of learning
    H J Lee
    Department of Psychological and Brain Sciences, Johns Hopkins University, 204 Ames Hall, 3400 North Charles Street, Baltimore, MD 21218, USA
    Eur J Neurosci 27:3043-9. 2008
    ..The results show that SNc-CeA communication is critical for processing prediction error information at the time of surprise, but neither SNc nor SNc-CeA communication is necessary to express that information as enhanced learning later...
  35. ncbi Cocaine makes actions insensitive to outcomes but not extinction: implications for altered orbitofrontal-amygdalar function
    Geoffrey Schoenbaum
    Department of Anatomy and Neurobiology, University of Maryland School of Medicine, 20 Penn Street, HSF 2 S251, Baltimore, MD 21201, USA
    Cereb Cortex 15:1162-9. 2005
    ....