Optogenetic Dissection of Basolateral Amygdala Contributions to Intertemporal Choice in Young and Aged Rats

Overview

Journal Elife

Specialty Biology

Date 2019 Apr 25

PMID 31017572

Citations 13

Authors

Caesar M Hernandez

Caitlin A Orsini

Chase C Labiste

Alexa-Rae Wheeler

Tyler W Ten Eyck

Matthew M Bruner

Todd J Sahagian

Scott W Harden

Charles J Frazier

Barry Setlow

Jennifer L Bizon

Affiliations

Soon will be listed here.

Abstract

Across species, aging is associated with an increased ability to choose delayed over immediate gratification. These experiments used young and aged rats to test the role of the basolateral amygdala (BLA) in intertemporal decision making. An optogenetic approach was used to inactivate the BLA in young and aged rats at discrete time points during choices between levers that yielded a small, immediate vs. a large, delayed food reward. BLA inactivation just prior to decisions attenuated impulsive choice in both young and aged rats. In contrast, inactivation during receipt of the small, immediate reward increased impulsive choice in young rats but had no effect in aged rats. BLA inactivation during the delay or intertrial interval had no effect at either age. These data demonstrate that the BLA plays multiple, temporally distinct roles during intertemporal choice, and show that the contribution of BLA to choice behavior changes across the lifespan.

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References

Evenden J, Ryan C . The pharmacology of impulsive behaviour in rats: the effects of drugs on response choice with varying delays of reinforcement. Psychopharmacology (Berl). 1996; 128(2):161-70. DOI: 10.1007/s002130050121. View

Hu X, Uhle F, Fliessbach K, Wagner M, Han Y, Weber B . Reduced future-oriented decision making in individuals with subjective cognitive decline: A functional MRI study. Alzheimers Dement (Amst). 2017; 6:222-231. PMC: 5376255. DOI: 10.1016/j.dadm.2017.02.005. View

Rubinow M, Juraska J . Neuron and glia numbers in the basolateral nucleus of the amygdala from preweaning through old age in male and female rats: a stereological study. J Comp Neurol. 2008; 512(6):717-25. PMC: 2647367. DOI: 10.1002/cne.21924. View

Boyle P, Yu L, Wilson R, Gamble K, Buchman A, Bennett D . Poor decision making is a consequence of cognitive decline among older persons without Alzheimer's disease or mild cognitive impairment. PLoS One. 2012; 7(8):e43647. PMC: 3423371. DOI: 10.1371/journal.pone.0043647. View

Hernandez C, Vetere L, Orsini C, McQuail J, Maurer A, Burke S . Decline of prefrontal cortical-mediated executive functions but attenuated delay discounting in aged Fischer 344 × brown Norway hybrid rats. Neurobiol Aging. 2017; 60:141-152. PMC: 5669385. DOI: 10.1016/j.neurobiolaging.2017.08.025. View

Jimura K, Myerson J, Hilgard J, Keighley J, Braver T, Green L . Domain independence and stability in young and older adults' discounting of delayed rewards. Behav Processes. 2011; 87(3):253-9. PMC: 3138910. DOI: 10.1016/j.beproc.2011.04.006. View

Samson R, Lester A, Duarte L, Venkatesh A, Barnes C . Emergence of β-Band Oscillations in the Aged Rat Amygdala during Discrimination Learning and Decision Making Tasks. eNeuro. 2017; 4(5). PMC: 5629614. DOI: 10.1523/ENEURO.0245-17.2017. View

Shadlen M, Shohamy D . Decision Making and Sequential Sampling from Memory. Neuron. 2016; 90(5):927-39. PMC: 4891701. DOI: 10.1016/j.neuron.2016.04.036. View

Fobbs W, Mizumori S . A framework for understanding and advancing intertemporal choice research using rodent models. Neurobiol Learn Mem. 2017; 139:89-97. PMC: 5407470. DOI: 10.1016/j.nlm.2017.01.004. View

10.

Mata R, Josef A, Samanez-Larkin G, Hertwig R . Age differences in risky choice: a meta-analysis. Ann N Y Acad Sci. 2011; 1235:18-29. PMC: 3332530. DOI: 10.1111/j.1749-6632.2011.06200.x. View

11.

Ghods-Sharifi S, St Onge J, Floresco S . Fundamental contribution by the basolateral amygdala to different forms of decision making. J Neurosci. 2009; 29(16):5251-9. PMC: 6665478. DOI: 10.1523/JNEUROSCI.0315-09.2009. View

12.

Mitchell M, Weiss V, Beas B, Morgan D, Bizon J, Setlow B . Adolescent risk taking, cocaine self-administration, and striatal dopamine signaling. Neuropsychopharmacology. 2013; 39(4):955-62. PMC: 3924529. DOI: 10.1038/npp.2013.295. View

13.

Hamilton K, Mitchell M, Wing V, Balodis I, Bickel W, Fillmore M . Choice impulsivity: Definitions, measurement issues, and clinical implications. Personal Disord. 2015; 6(2):182-98. PMC: 4535726. DOI: 10.1037/per0000099. View

14.

Burgos-Robles A, Kimchi E, Izadmehr E, Porzenheim M, Ramos-Guasp W, Nieh E . Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment. Nat Neurosci. 2017; 20(6):824-835. PMC: 5448704. DOI: 10.1038/nn.4553. View

15.

Green L, Myerson J, Ostaszewski P . Discounting of delayed rewards across the life span: age differences in individual discounting functions. Behav Processes. 2014; 46(1):89-96. DOI: 10.1016/S0376-6357(99)00021-2. View

16.

Lockenhoff C, ODonoghue T, Dunning D . Age differences in temporal discounting: the role of dispositional affect and anticipated emotions. Psychol Aging. 2011; 26(2):274-284. DOI: 10.1037/a0023280. View

17.

Mariano T, Bannerman D, McHugh S, Preston T, Rudebeck P, Rudebeck S . Impulsive choice in hippocampal but not orbitofrontal cortex-lesioned rats on a nonspatial decision-making maze task. Eur J Neurosci. 2009; 30(3):472-84. PMC: 2777256. DOI: 10.1111/j.1460-9568.2009.06837.x. View

18.

Samanez-Larkin G, Mata R, Radu P, Ballard I, Carstensen L, McClure S . Age Differences in Striatal Delay Sensitivity during Intertemporal Choice in Healthy Adults. Front Neurosci. 2011; 5:126. PMC: 3217179. DOI: 10.3389/fnins.2011.00126. View

19.

Burke S, Thome A, Plange K, Engle J, Trouard T, Gothard K . Orbitofrontal cortex volume in area 11/13 predicts reward devaluation, but not reversal learning performance, in young and aged monkeys. J Neurosci. 2014; 34(30):9905-16. PMC: 4107407. DOI: 10.1523/JNEUROSCI.3918-13.2014. View

20.

Simon N, LaSarge C, Montgomery K, Williams M, Mendez I, Setlow B . Good things come to those who wait: attenuated discounting of delayed rewards in aged Fischer 344 rats. Neurobiol Aging. 2008; 31(5):853-62. PMC: 2866647. DOI: 10.1016/j.neurobiolaging.2008.06.004. View