Abstract
Rationale
The rat cognitive effort task (rCET), a rodent model of cognitive rather than physical effort, requires animals to choose between an easy or hard visuospatial discrimination, with a correct hard choice more highly rewarded. Like in humans, there is stable individual variation in choice behavior. In previous reports, animals were divided into two groups—workers and slackers—based on their mean preference for the harder option. Although these groups differed in their response to pharmacological challenges, the rationale for using this criterion for grouping was not robust.
Methods
We collated experimental data from multiple cohorts of male and female rats performing the rCET and used a model-based framework combining drift diffusion modeling with cluster analysis to identify the decision-making processes underlying variation in choice behavior.
Results
We verified that workers and slackers are statistically different groups but also found distinct intra-group profiles. These subgroups exhibited dissociable performance during the attentional phase, linked to distinct decision-making profiles during choice. Reanalysis of previous pharmacology data using this model-based framework showed that serotonergic drug effects were explained by changes in decision boundaries and non-decision times, while scopolamine’s effects were driven by changes in decision starting points and rates of evidence accumulation.
Conclusions
Modeling revealed the decision-making processes that are associated with cognitive effort costs, and how these differ across individuals. Reanalysis of drug data provided insight into the mechanisms through which different neurotransmitter systems impact cognitively effortful attention and decision-making processes, with relevance to multiple psychiatric disorders.
Similar content being viewed by others
Data Availability
Datasets analysed for the current study are available from the corresponding author upon request.
References
Adams WK, Barkus C, Ferland JN, Sharp T, Winstanley CA (2017) Pharmacological evidence that 5-HT2C receptor blockade selectively improves decision making when rewards are paired with audiovisual cues in a rat gambling task. Psychopharmacology 234(20):3091–3104. https://doi.org/10.1007/s00213-017-4696-4
Chong TT, Apps M, Giehl K, Sillence A, Grima LL, Husain M (2017) Neurocomputational mechanisms underlying subjective valuation of effort costs. PLoS Biol 15(2):e1002598. https://doi.org/10.1371/journal.pbio.1002598
Cocker PJ, Hosking JG, Benoit J, Winstanley CA (2012) Sensitivity to cognitive effort mediates psychostimulant effects on a novel rodent cost/benefit decision-making task. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 37(8):1825–1837. https://doi.org/10.1038/npp.2012.30
Der-Avakian A, Barnes SA, Markou A, Pizzagalli DA (2016) Translational assessment of reward and motivational deficits in psychiatric disorders. Curr Top Behav Neurosci 28:231–262. https://doi.org/10.1007/7854_2015_5004
Dixon ML, Christoff K (2012) The decision to engage cognitive control is driven by expected reward-value: neural and behavioral evidence. PLoS ONE 7(12):e51637. https://doi.org/10.1371/journal.pone.0051637
Dutilh G, Rieskamp J (2016) Comparing perceptual and preferential decision making. Psychon Bull Rev 23(3):723–737. https://doi.org/10.3758/s13423-015-0941-1
Fletcher PJ, Tampakeras M, Sinyard J, Higgins GA (2007) Opposing effects of 5-HT(2A) and 5-HT(2C) receptor antagonists in the rat and mouse on premature responding in the five-choice serial reaction time test. Psychopharmacology 195(2):223–234. https://doi.org/10.1007/s00213-007-0891-z
Fobbs WC, Mizumori SJ (2014) Cost-benefit decision circuitry: proposed modulatory role for acetylcholine. Prog Mol Biol Transl Sci 122:233–261. https://doi.org/10.1016/B978-0-12-420170-5.00009-X
Gleichgerrcht E, Ibáñez A, Roca M, Torralva T, Manes F (2010) Decision-making cognition in neurodegenerative diseases. Nat Rev Neurol 6(11):611–623. https://doi.org/10.1038/nrneurol.2010.148
Goschke T (2014) Dysfunctions of decision-making and cognitive control as transdiagnostic mechanisms of mental disorders: advances, gaps, and needs in current research. Int J Methods Psychiatr Res 23(Suppl 1):41–57. https://doi.org/10.1002/mpr.1410
Hales CA, Robinson ES, Houghton CJ (2016) Diffusion modelling reveals the decision making processes underlying negative judgement bias in rats. PLoS ONE 11(3):e0152592. https://doi.org/10.1371/journal.pone.0152592
Hales CA, Houghton CJ, Robinson ESJ (2017) Behavioural and computational methods reveal differential effects for how delayed and rapid onset antidepressants effect decision making in rats. European Neuropsychopharmacology: the Journal of the European College of Neuropsychopharmacology 27(12):1268–1280. https://doi.org/10.1016/j.euroneuro.2017.09.008
Haushofer J, Fehr E (2014) On the psychology of poverty. Science (New York, N.Y.) 344(6186):862–867. https://doi.org/10.1126/science.1232491
Homberg JR (2012) Serotonin and decision making processes. Neurosci Biobehav Rev 36(1):218–236. https://doi.org/10.1016/j.neubiorev.2011.06.001
Hosking JG, Lam FC, Winstanley CA (2014) Nicotine increases impulsivity and decreases willingness to exert cognitive effort despite improving attention in “slacker” rats: insights into cholinergic regulation of cost/benefit decision making. PLoS ONE 9(10):e111580. https://doi.org/10.1371/journal.pone.0111580
Hosking JG, Floresco SB, Winstanley CA (2015) Dopamine antagonism decreases willingness to expend physical, but not cognitive, effort: a comparison of two rodent cost/benefit decision-making tasks. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 40(4):1005–1015. https://doi.org/10.1038/npp.2014.285
Hosking JG, Cocker PJ, Winstanley CA (2016) Prefrontal cortical inactivations decrease willingness to expend cognitive effort on a rodent cost/benefit decision-making task. Cereb Cortex (New York, N.Y.: 1991) 26(4):1529–1538. https://doi.org/10.1093/cercor/bhu321
Kool W, McGuire JT, Rosen ZB, Botvinick MM (2010) Decision making and the avoidance of cognitive demand. J Exp Psychol Gen 139(4):665–682. https://doi.org/10.1037/a0020198
McGuire JT, Botvinick MM (2010) Prefrontal cortex, cognitive control, and the registration of decision costs. Proc Natl Acad Sci USA 107(17):7922–7926. https://doi.org/10.1073/pnas.0910662107
Milosavljevic M, Malmaud J, Huth A, Koch C, Rangel A (2010) The drift diffusion model can account for the accuracy and reaction time of value-based choices under high and low time pressure. Judgm Decis Mak 5(6):437–449
Nelder JA, Mead R (1965) A simplex method for function minimization. Comput J 7:308–313. https://doi.org/10.1093/comjnl/7.4.308
Ratcliff R (1978) A theory of memory retrieval. Psychol Rev 85:59–108
Ratcliff R, Tuerlinckx F (2002) Estimating parameters of the diffusion model: approaches to dealing with contaminant reaction times and parameter variability. Psychon Bull Rev 9(3):438–481. https://doi.org/10.3758/bf03196302
Reddy LF, Horan WP, Barch DM, Buchanan RW, Dunayevich E, Gold JM, Lyons N, Marder SR, Treadway MT, Wynn JK, Young JW, Green MF (2015) Effort-based decision-making paradigms for clinical trials in schizophrenia: part 1—psychometric characteristics of 5 paradigms. Schizophr Bull 41(5):1045–1054. https://doi.org/10.1093/schbul/sbv089
Robbins TW (2002) The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology 163(3–4):362–380. https://doi.org/10.1007/s00213-002-1154-7
Sharp T, Barnes NM (2020) Central 5-HT receptors and their function; present and future. Neuropharmacology 177:108155. https://doi.org/10.1016/j.neuropharm.2020.108155
Silveira MM (2018) Investigating the neurobiology regulating cognitive effort allocation using a rodent model of cost/benefit decision making. Doctoral dissertation, The University of British Columbia. https://doi.org/10.14288/1.0372368
Silveira MM, Adams WK, Morena M, Hill MN, Winstanley CA (2017) Δ9-Tetrahydrocannabinol decreases willingness to exert cognitive effort in male rats. J Psychiatry Neurosci: JPN 42(2):131–138. https://doi.org/10.1503/jpn.150363
Silveira MM, Tremblay M, Winstanley CA (2018) Dissociable contributions of dorsal and ventral striatal regions on a rodent cost/benefit decision-making task requiring cognitive effort. Neuropharmacol 137:322–331. https://doi.org/10.1016/j.neuropharm.2018.04.025
Silveira MM, Wittekindt SN, Mortazavi L, Hathaway BA, Winstanley CA (2020) Investigating serotonergic contributions to cognitive effort allocation, attention, and impulsive action in female rats. J Psychopharmacol 34(4):452–466. https://doi.org/10.1177/0269881119896043
Silveira MM, Wittekindt SN, Ebsary S, Winstanley CA (2021) Evaluation of cognitive effort in rats is not critically dependent on ventrolateral orbitofrontal cortex. Eur J Neurosci 53(3):852–860. https://doi.org/10.1111/ejn.14940
Tajima S, Drugowitsch J, Pouget A (2016) Optimal policy for value-based decision-making. Nat Commun 7:12400. https://doi.org/10.1038/ncomms12400
Voss A, Voss J (2007) Fast-dm: a free program for efficient diffusion model analysis. Behav Res Methods 39(4):767–775. https://doi.org/10.3758/bf03192967
Voss A, Voss J (2008) A fast numerical algorithm for the estimation of diffusion model parameters. J Math Psychol 52:1–9. https://doi.org/10.1016/j.jmp.2007.09.005
Voss A, Voss J, Klauer KC (2010) Separating response-execution bias from decision bias: arguments for an additional parameter in Ratcliff’s diffusion model. Br J Math Stat Psychol 63(Pt 3):539–555. https://doi.org/10.1348/000711009X477581
Voss A, Nagler M, Lerche V (2013) Diffusion models in experimental psychology: a practical introduction. Exp Psychol 60(6):385–402. https://doi.org/10.1027/1618-3169/a000218
Voss A, Voss J, Lerche V (2015) Assessing cognitive processes with diffusion model analyses: a tutorial based on fast-dm-30. Front Psychol 6:336. https://doi.org/10.3389/fpsyg.2015.00336
Westbrook A, Kester D, Braver TS (2013) What is the subjective cost of cognitive effort? Load, trait, and aging effects revealed by economic preference. PLoS ONE 8(7):e68210. https://doi.org/10.1371/journal.pone.0068210
Winstanley CA, Chudasama Y, Dalley JW, Theobald DE, Glennon JC, Robbins TW (2003) Intra-prefrontal 8-OH-DPAT and M100907 improve visuospatial attention and decrease impulsivity on the five-choice serial reaction time task in rats. Psychopharmacology 167(3):304–314. https://doi.org/10.1007/s00213-003-1398-x
Winstanley CA, Theobald DE, Dalley JW, Glennon JC, Robbins TW (2004) 5-HT2A and 5-HT2C receptor antagonists have opposing effects on a measure of impulsivity: interactions with global 5-HT depletion. Psychopharmacology 176(3–4):376–385. https://doi.org/10.1007/s00213-004-1884-9
Acknowledgements
The experimental work took place at a UBC campus situated on the traditional, ancestral, and unceded land of the xʷməθkʷəy̓əm (Musqueam), sə̓lílwətaʔɬSelilwitulh (Tsleil-Waututh), and Sḵwx̱wú7mesh (Squamish) peoples. We acknowledge and are grateful for their stewardship of this land for thousands of years.
Funding
This work was supported by a Discovery Grant awarded to CAW from the Natural Sciences and Engineering Research Council of Canada (NSERC; RGPIN-2017–05006). CAH was supported by a Michael Smith Health Research BC Trainee Award (#RT-2020–0564). MMS was supported by an NSERC Doctoral Award. BAH was supported by a Canadian Institutes for Health Research Doctoral Award.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Hales, C.A., Silveira, M.M., Calderhead, L. et al. Insight into differing decision-making strategies that underlie cognitively effort-based decision making using computational modeling in rats. Psychopharmacology 241, 947–962 (2024). https://doi.org/10.1007/s00213-023-06521-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00213-023-06521-5