Stress influences various types of memory, but its effects on other cognitive functions are relatively unknown. We investigated the effects of uncontrollable stress on subsequent decision-making in rats, using a computer vision-based water foraging choice task. Stress impaired the animals&#x27; ability to bias their responses toward the larger reward when transitioning from equal to unequal quantities, and this stress effect was dependent on the amygdala

Jeansok J. Kim

Lauren K. Jones

Taejib Yoon

English

Nature Precedings

  
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Stress impairs decision-making in rats 
 
 
Lauren K. Jones1, Taejib Yoon1, and Jeansok J. Kim1,2 
 
 
1Department of Psychology and 2Program in Neurobiology & Behavior, 335 Guthrie Hall, 
University of Washington, Seattle, Washington 98195-1525, USA. 
 
 
Corresponding author:  Jeansok J. Kim, Department of Psychology, Guthrie Hall, University of 
Washington, Seattle, WA 98195-1525, Tel: (206) 616-2685; Fax: (206) 685-3157; E-mail: 
jeansokk@u.washington.edu 
 
 
 
Number of words in the abstract: 65  
Number of words in the main text: 1197 (including abstract, references and figure legends)  
Number of references: 12 
Number of figures: 2 
 
 
Running head: Stress and decision-making 
  
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Stress influences various types of memory, but its effects on other cognitive functions are 
relatively unknown.  We investigated the effects of uncontrollable stress on subsequent 
decision-making in rats, using a computer vision-based water foraging choice task.  Stress 
impaired the animals’ ability to bias their responses toward the larger reward when 
transitioning from equal to unequal quantities, and this stress effect was dependent on the 
amygdala.   
  
It is now well documented that stress, a biologically significant and pervasive environmental 
factor, can produce alterations in brain-memory systems1,2.  In humans, impairments in verbal 
recall tasks have been observed in posttraumatic stress disorder patients3, and in healthy 
individuals exposed to stress4.  In rodents, stress impedes spatial5 memory, while potentiating 
aversive conditioning6,7.  Further, various stress-associated neurobiological changes have been 
identified in brain structures (e.g., hippocampus1,2, medial prefrontal cortex8, amygdala9) 
subserving memory functions.   
Although stress effects on memory have been extensively studied, far less is known about 
whether (and in what manner) stress influences other cognitive functions.  The present study 
investigated the effects of acute, uncontrollable stress on subsequent decision-making 
performance in rats.  Decision-making was assessed using an automated Figure-8 maze in 
  
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which rats were motivated to forage for water rewards in two different locations under equal 
and unequal quantity conditions (Fig. 1).  Detailed methods are provided in Supplementary 
Methods online. 
Rats readily learned to forage for water, and when left (L) and right (R) sides of the maze 
provided equal quantity and probability (0.04 ml, 80%) of water, animals made comparable 
numbers of L/R visits that were stable across three baseline days (Fig. 2a).  When the reward 
volume on one side only was tripled (0.12 ml, 80%), unstressed (‘control’) animals readily made 
more visits to the larger reward.  In contrast, (‘stress’) rats that experienced 60 min 
restraint+60 intermittent tailshocks on the previous day displayed a slower rate of bias toward 
the larger reward than did the controls (P = .007).  Although stress rats eventually showed a 
reliable bias toward the larger reward by the fourth day of bias testing (P = .006), even after six 
days, their bias (132 + 7.2%, means + s.e.m.) did not reach the level of controls’ third day bias 
(181 + 12.5%).  Animals that received daily corticosterone (‘CORT’) injections prior to testing 
chose the larger reward more frequently (173 + 6.7%, Bias day 3), and did not differ from the 
controls (P > .9).  Animals with their amygdalae inactivated during stress (‘AMYG’), via 
infusions of the GABAA receptor agonist muscimol (Supplementary Fig. 1), behaved like controls 
(P > .9) and visited the larger reward more frequently (174 + 13.0%, Bias day 3). 
  
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We then examined whether stress altered motor, motivation or reference memory that 
hindered the ability to bias responses toward the larger reward.  The latency to complete the 
first bias test (Fig. 2b) showed a trend of stress animals finishing faster than the other groups (P 
= .154).  Stress also did not impair the animals’ reference memory: after making a L or R choice, 
stressed animals readily re-entered the center runway to start the next trial, whereas other 
groups more often investigated the other side before re-entering the center runway, particularly 
as bias testing progressed (P = .032, group x day; Supplementary Fig. 2a).  
Our results indicate that rats clearly demonstrate the capacity to change their foraging 
behavior to acquire a larger reward, and that such decision-making is vulnerable to stress.  This 
effect was not due to any lingering post-stress motivational or motor effects, as the latency to 
complete the bias test did not differ between stress and control rats.  Daily corticosterone 
injections did not interfere with this task, indicating that corticosterone elevation alone cannot 
reproduce behavioral stress effects on decision-making.  Similar to previous stress-memory 
studies2,6, amygdalar inactivation effectively blocked stress effects on decision-making.  This 
suggests that the amygdala plays a crucial role in mediating stress effects across different 
cognitive domains.   
Although stress might have directly affected the brain systems underlying decision-making, 
thus altering ensuing behavior, alternate possibilities should be considered.  For instance, the 
  
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impairment of decision-making might be a consequence of stress effects on spatial working 
memory.  The stress paradigm used here is known to alter hippocampal synaptic plasticity2 and 
hinder spatial memory5.  Therefore, contributions of stress-associated changes in learning 
cannot be excluded.  Another possibility is that the “prudent” foraging behavior after stress is 
to maintain habitual behavior even if deviation may result in higher benefit.  The fact that 
stressed rats less frequently investigated other parts of the maze is consistent with this 
explanation.  The evolutionary history of the animal in foraging behavior10 is clearly a crucial 
factor to be considered with regard to decision-making and adaptive behavioral responses to 
stress.  It is also possible that stress disrupted the reward circuitry and impaired the ability to 
discriminate between the two reward values (Supplementary Fig. 2b), in which case stress 
effects on a dopamine-related reward circuit11 need to be explored.   
If acute, uncontrollable stress influences subsequent decision-making, what is the neural 
basis for this effect?  To address this, future studies need to investigate brain structures 
implicated in decision-making, including the prefrontal and the parietal cortices12, for their 
susceptibility to stress.  Regardless, the present findings, to our knowledge, provide the first 
direct evidence that uncontrollable stress impairs decision-making performance in rats and that 
this effect is dependent upon amygdalar activity during stress. 
  
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References 
1.  McEwen, B.S. & Sapolsky, R.M. Curr. Opin. Neurobiol. 5, 205-216 (1995).  
2. Kim, J.J. & Diamond, D.M. Nat. Rev. Neurosci. 3, 453-462 (2002). 
3. Bremner, J.D. et al. Am. J. Psychiatry 152, 973-981 (1995). 
4.  Lupien, S.J. et al. J. Clin. Endocrinol. Metab. 82, 2070-2075 (1997).  
5. Diamond, D.M. & Rose, G.M. Ann. NY. Acad. Sci. 746, 411-414 (1994). 
6. Waddell, J., Bangasser, D.A. & Shors, T.J. J. Neurosci. 28, 5290-5294 (2008). 
7. Maier, S.F., Grahn, R.E. & Watkins, L.R. et al. Behav. Neurosci. 109, 404-412 (1995). 
8.  Arnsten, A.F.T. & Goldman-Rakic, P.S. Arch. Gen. Psychiatry 55, 362-368 (1998) 
9. Vyas, A., Bernal, S. & Chattarji, S. Brain Res. 965, 290-294 (2003). 
10. Pyke, G.H. Ann. Rev. Ecol. Syst. 15, 523-575 (1984). 
11. Schultz, W.P., Dayan, P. & Montague, R.P. Science 275, 1593-1599 (1997).   
12. Gold, J.I. & Shadlen, M.N. Ann. Rev. Neurosci. 30, 535-574 (2007).  
  
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Figure legends 
 
Figure 1.  Decision-making task.  (a) Rats were trained to forage for water on a figure-eight 
maze.  A computer algorithm controlled the four gates (rectangles) and water delivery (blue 
circles), while tracking the animal’s location.  During baseline testing, left and right rewards 
were equal in volume (V) and probability (P).  During bias testing, one reward 
(counterbalanced) was increased in volume relative to the other reward.  (b) Example visit 
maps of rats during baseline, control and stress conditions (40 laps each).  
 
Figure 2.  Stress and decision-making.  (a) All groups showed comparable visits to left and 
right rewards during baseline testing.  When transitioning from equal to unequal reward trials, 
stressed rats (n = 7) displayed an impaired ability to bias their responses toward the larger 
reward side compared to control (n = 10), AMYG (n = 7) and CORT (n = 7) rats, F6,54 = 4.142, P 
= .002, group x bias day interaction.  (b) During bias testing, all groups took similar latencies to 
complete the 40 laps.
  
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Acknowledgments 
This study was supported by R01 MH64457 and the University of Washington Royalty 
Research Fellowship to J.J.K.  We thank Andrew R. Graham for the figure-8 maze control and 
analyses programs, and Valentino C. Garcia and Joseph Reichert for their assistance in the 
experiment.   
 
Author contributions 
J.J.K., L.K.J., and T.Y. designed research; L.K.J., T.Y., and J.J.K. performed research; L.K.J., T.Y., 
and J.J.K. analyzed data; and J.J.K. and L.K.J. wrote the paper. 
  
Financial Disclosures 
The authors declare that they have no competing financial interests. 
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Stress impairs decision-making in rats

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Stress impairs decision-making in rats

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