Neurons in the Primate Medial Basal Forebrain Signal Combined Information About Reward Uncertainty, Value, and Punishment Anticipation

Overview

Journal J Neurosci

Specialty Neurology

Date 2015 May 15

PMID 25972172

Citations 33

Authors

Ilya E Monosov

David A Leopold

Okihide Hikosaka

Affiliations

Soon will be listed here.

Abstract

It has been suggested that the basal forebrain (BF) exerts strong influences on the formation of memory and behavior. However, what information is used for the memory-behavior formation is unclear. We found that a population of neurons in the medial BF (medial septum and diagonal band of Broca) of macaque monkeys encodes a unique combination of information: reward uncertainty, expected reward value, anticipation of punishment, and unexpected reward and punishment. The results were obtained while the monkeys were expecting (often with uncertainty) a rewarding or punishing outcome during a Pavlovian procedure, or unexpectedly received an outcome outside the procedure. In vivo anterograde tracing using manganese-enhanced MRI suggested that the major recipient of these signals is the intermediate hippocampal formation. Based on these findings, we hypothesize that the medial BF identifies various contexts and outcomes that are critical for memory processing in the hippocampal formation.

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References

Schultz W, Dayan P, Montague P . A neural substrate of prediction and reward. Science. 1997; 275(5306):1593-9. DOI: 10.1126/science.275.5306.1593. View

Monosov I, Hikosaka O . Regionally distinct processing of rewards and punishments by the primate ventromedial prefrontal cortex. J Neurosci. 2012; 32(30):10318-30. PMC: 3438659. DOI: 10.1523/JNEUROSCI.1801-12.2012. View

Le Pelley M, Beesley T, Griffiths O . Overt attention and predictiveness in human contingency learning. J Exp Psychol Anim Behav Process. 2011; 37(2):220-9. DOI: 10.1037/a0021384. View

McCoy A, Platt M . Risk-sensitive neurons in macaque posterior cingulate cortex. Nat Neurosci. 2005; 8(9):1220-7. DOI: 10.1038/nn1523. View

De Rosa E, Hasselmo M . Muscarinic cholinergic neuromodulation reduces proactive interference between stored odor memories during associative learning in rats. Behav Neurosci. 2000; 114(1):32-41. View

De Rosa E, Desmond J, Anderson A, Pfefferbaum A, Sullivan E . The human basal forebrain integrates the old and the new. Neuron. 2004; 41(5):825-37. DOI: 10.1016/s0896-6273(04)00080-7. View

Simmons J, Saad Z, Lizak M, Ortiz M, Koretsky A, Richmond B . Mapping prefrontal circuits in vivo with manganese-enhanced magnetic resonance imaging in monkeys. J Neurosci. 2008; 28(30):7637-47. PMC: 2683620. DOI: 10.1523/JNEUROSCI.1488-08.2008. View

Eschenko O, Canals S, Simanova I, Logothetis N . Behavioral, electrophysiological and histopathological consequences of systemic manganese administration in MEMRI. Magn Reson Imaging. 2010; 28(8):1165-74. DOI: 10.1016/j.mri.2009.12.022. View

Espana R, Berridge C . Organization of noradrenergic efferents to arousal-related basal forebrain structures. J Comp Neurol. 2006; 496(5):668-83. DOI: 10.1002/cne.20946. View

10.

Vertes R . Brainstem afferents to the basal forebrain in the rat. Neuroscience. 1988; 24(3):907-35. DOI: 10.1016/0306-4522(88)90077-2. View

11.

McNally G, Johansen J, Blair H . Placing prediction into the fear circuit. Trends Neurosci. 2011; 34(6):283-92. PMC: 4245078. DOI: 10.1016/j.tins.2011.03.005. View

12.

Damasio A, Graff-Radford N, Eslinger P, Damasio H, Kassell N . Amnesia following basal forebrain lesions. Arch Neurol. 1985; 42(3):263-71. DOI: 10.1001/archneur.1985.04060030081013. View

13.

Semba K . Multiple output pathways of the basal forebrain: organization, chemical heterogeneity, and roles in vigilance. Behav Brain Res. 2000; 115(2):117-41. DOI: 10.1016/s0166-4328(00)00254-0. View

14.

Baxter M, Holland P, Gallagher M . Disruption of decrements in conditioned stimulus processing by selective removal of hippocampal cholinergic input. J Neurosci. 1997; 17(13):5230-6. PMC: 6573295. View

15.

Simon A, Poindessous-Jazat F, Dutar P, Epelbaum J, Bassant M . Firing properties of anatomically identified neurons in the medial septum of anesthetized and unanesthetized restrained rats. J Neurosci. 2006; 26(35):9038-46. PMC: 6675331. DOI: 10.1523/JNEUROSCI.1401-06.2006. View

16.

Loewenstein G, Weber E, Hsee C, Welch N . Risk as feelings. Psychol Bull. 2001; 127(2):267-86. DOI: 10.1037/0033-2909.127.2.267. View

17.

Lisman J, Grace A . The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron. 2005; 46(5):703-13. DOI: 10.1016/j.neuron.2005.05.002. View

18.

Suzuki W, Miller E, DeSimone R . Object and place memory in the macaque entorhinal cortex. J Neurophysiol. 1997; 78(2):1062-81. DOI: 10.1152/jn.1997.78.2.1062. View

19.

Baxter M, Bucci D . Selective immunotoxic lesions of basal forebrain cholinergic neurons: twenty years of research and new directions. Behav Neurosci. 2013; 127(5):611-8. DOI: 10.1037/a0033781. View

20.

Iglesias S, Mathys C, Brodersen K, Kasper L, Piccirelli M, den Ouden H . Hierarchical prediction errors in midbrain and basal forebrain during sensory learning. Neuron. 2013; 80(2):519-30. DOI: 10.1016/j.neuron.2013.09.009. View