Altering gain of the infralimbic-to-accumbens shell circuit alters economically dissociable decision-making algorithms

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Abstract

The nucleus accumbens shell (NAcSh) is involved in reward valuation. Excitatory projections from infralimbic cortex (IL) to NAcSh undergo synaptic remodeling in rodent models of addiction and enable the extinction of disadvantageous behaviors. However, how the strength of synaptic transmission of the IL–NAcSh circuit affects decision-making information processing and reward valuation remains unknown, particularly because these processes can conflict within a given trial and particularly given recent data suggesting that decisions arise from separable information-processing algorithms. The approach of many neuromodulation studies is to disrupt information flow during on-going behaviors; however, this limits the interpretation of endogenous encoding of computational processes. Furthermore, many studies are limited by the use of simple behavioral tests of value which are unable to dissociate neurally distinct decision-making algorithms. We optogenetically altered the strength of synaptic transmission between glutamatergic IL–NAcSh projections in mice trained on a neuroeconomic task capable of separating multiple valuation processes. We found that induction of long-term depression in these synapses produced lasting changes in foraging processes without disrupting deliberative processes. Mice displayed inflated reevaluations to stay when deciding whether to abandon continued reward-seeking investments but displayed no changes during initial commitment decisions. We also developed an ensemble-level measure of circuit-specific plasticity that revealed individual differences in foraging valuation tendencies. Our results demonstrate that alterations in projection-specific synaptic strength between the IL and the NAcSh are capable of augmenting self-control economic valuations within a particular decision-making modality and suggest that the valuation mechanisms for these multiple decision-making modalities arise from different circuits.

Original languageEnglish (US)
Pages (from-to)E6347-E6355
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number27
DOIs
StatePublished - Jul 3 2018

Bibliographical note

Funding Information:
Behavior. Mice implanted with virus-infected optic fiber in the IL/NAcSh were trained on the Restaurant Row task for 70 consecutive days before undergoing a series of acute optogenetic stimulation protocols delivered outside behavioral testing (SI Appendix, Supplementary Materials and Methods) ACKNOWLEDGMENTS. We thank members of the A.D.R. and M.J.T. laboratories, the MnDRIVE Optogenetics Core of the University of Minnesota, Dr. Patrick Rothwell, Dr. Michael Benneyworth, Dr. Manuel Esguerra, Cody Walters, Brendan Hasz, and Caleb Fink for helpful discussions and technical assistance; Ethan Huffington for assistance with surgeries; and Amber McLaughlin, Colleen Hutchison, Madeline Jones, Frank Valdes, Maya Smith, Peter Nicholson, Delfina Mancebo, and Nolan Trevino for help with mouse testing. This research was supported by National Institute on Drug Abuse Grants R01 DA019666, R01 DA030672, R01 DA052808, and F30 DA043326; National Institute of Mental Health Grants R01 MH080318 and R01 MH112688; National Institute of General Medical Sciences Grants 5T32GM008244-25 and 5T32GM008471-22; University of Minnesota MnDRIVE Neuromodulation Research Fellowship; and the Breyer-Longden Family Research Foundation.

Funding Information:
We thank members of the A.D.R. and M.J.T. laboratories, the MnDRIVE Optogenetics Core of the University of Minnesota, Dr. Patrick Rothwell, Dr. Michael Benneyworth, Dr. Manuel Esguerra, Cody Walters, Brendan Hasz, and Caleb Fink for helpful discussions and technical assistance; Ethan Huffington for assistance with surgeries; and Amber McLaughlin, Colleen Hutchison, Madeline Jones, Frank Valdes, Maya Smith, Peter Nicholson, Delfina Mancebo, and Nolan Trevino for help with mouse testing. This research was supported by National Institute on Drug Abuse Grants R01 DA019666, R01 DA030672, R01 DA052808, and F30 DA043326; National Institute of Mental Health Grants R01 MH080318 and R01 MH112688; National Institute of General Medical Sciences Grants 5T32GM008244-25 and 5T32GM008471-22; University of Minnesota MnDRIVE Neuromodulation Research Fellowship; and the Breyer-Longden Family Research Foundation.

Publisher Copyright:
© 2018 National Academy of Sciences. All Rights Reserved.

Keywords

  • Decision-making
  • Mice
  • Neuroeconomics
  • Optogenetics
  • Plasticity

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