Role of substantia nigra-amygdala connections in surprise-induced enhancement of attention

Hongjoo J. Lee, Jina M. Youn, Mary J. O, Michela Gallagher, Peter C Holland

Research output: Contribution to journalArticle

Abstract

Coding of prediction error by midbrain dopamine neurons has been examined extensively in the framework of associative learning theory. Most of this research has focused on the role of prediction error in determining the reinforcement value of unconditioned stimuli: poorly predicted ("surprising") outcomes are more effective reinforcers and produce a greater dopamine response than well predicted outcomes. However, surprise also enhances attention to cues that signal poorly predicted outcomes. Previous reports from our laboratories demonstrated that circuitry, including the amygdala central nucleus (CeA), the cholinergic neurons of the substantia innominata/nucleus basalis region, and their innervation of the posterior parietal cortex, is critical to these surprise-induced enhancements of attention in associative learning. The present study considered the origin of prediction error information important for the operation of this system by examining the effects of disrupting communication between the midbrain substantia nigra pars compacta (SNc) and the CeA. Rats received unilateral lesions of the SNc and lesions of the CeA in either the contralateral or ipsilateral hemisphere. Contralateral lesions eliminated the surprise-induced enhancement of attention and learning that was displayed by rats with ipsilateral control lesions. 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.

Original languageEnglish (US)
Pages (from-to)6077-6081
Number of pages5
JournalJournal of Neuroscience
Volume26
Issue number22
DOIs
StatePublished - 2006

Fingerprint

Substantia Nigra
Amygdala
Mesencephalon
Learning
Dopaminergic Neurons
Substantia Innominata
Communication
Parietal Lobe
Cholinergic Neurons
Cholinergic Agents
Cues
Dopamine
Research
Pars Compacta

Keywords

  • Amygdala central nucleus
  • Associative learning
  • Attention
  • Prediction error
  • Substantia nigra
  • Surprise

ASJC Scopus subject areas

  • Neuroscience(all)
  • Medicine(all)

Cite this

Role of substantia nigra-amygdala connections in surprise-induced enhancement of attention. / Lee, Hongjoo J.; Youn, Jina M.; O, Mary J.; Gallagher, Michela; Holland, Peter C.

In: Journal of Neuroscience, Vol. 26, No. 22, 2006, p. 6077-6081.

Research output: Contribution to journalArticle

Lee, Hongjoo J. ; Youn, Jina M. ; O, Mary J. ; Gallagher, Michela ; Holland, Peter C. / Role of substantia nigra-amygdala connections in surprise-induced enhancement of attention. In: Journal of Neuroscience. 2006 ; Vol. 26, No. 22. pp. 6077-6081.
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