Advanced search
Publication Cover
Spatial Cognition & Computation
An Interdisciplinary Journal
Volume 24, 2024 - Issue 3
Submit an article Journal homepage
109
Views
1
CrossRef citations to date
0
Altmetric
Research Article

Resilience of navigation strategy and efficiency to the impact of acute stress

Alexander P. Boonea Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USACorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-0367-2887View further author information
ORCID Icon,
Tom Bullocka Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USA;b Institute for Collaborative Biotechnologies, University of California, Santa Barbara, CA, USAView further author information
,
Mary H. MacLeana Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USA;b Institute for Collaborative Biotechnologies, University of California, Santa Barbara, CA, USAView further author information
,
Tyler Santandera Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USA;b Institute for Collaborative Biotechnologies, University of California, Santa Barbara, CA, USAView further author information
,
Jamie Raymera Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USAView further author information
,
Alexander Stubera Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USAView further author information
,
Liann Jimmonsa Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USAView further author information
,
Gold N. Okafora Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USAView further author information
,
Scott T. Graftona Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USA;b Institute for Collaborative Biotechnologies, University of California, Santa Barbara, CA, USA;c Graduate Program in Dynamical Neuroscience, University of California, Santa Barbara, CA, USAView further author information
,
Michael B. Millera Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USA;b Institute for Collaborative Biotechnologies, University of California, Santa Barbara, CA, USA;c Graduate Program in Dynamical Neuroscience, University of California, Santa Barbara, CA, USAView further author information
,
Barry Giesbrechta Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USA;b Institute for Collaborative Biotechnologies, University of California, Santa Barbara, CA, USA;c Graduate Program in Dynamical Neuroscience, University of California, Santa Barbara, CA, USAView further author information
&
Mary Hegartya Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA, USA;c Graduate Program in Dynamical Neuroscience, University of California, Santa Barbara, CA, USAView further author information
 show all
Pages 195-226 | Published online: 26 Feb 2024

References

  • Ament, W., & Verkerke, G. J. (2009). Exercise and fatigue. Sports Medicine, 39, 389–422.
  • Andreano, J. M., & Cahill, L. (2006). Glucocorticoid release and memory consolidation in men and women. Psychological Science, 17(6), 466–470. https://doi.org/10.1111/j.1467-9280.2006.01729.x
  • Birkett, M. A. (2011). The trier social stress test protocol for inducing psychological stress. Journal of Visualized Experiments: JoVE, 56(56), e3238. https://doi.org/10.3791/3238
  • Bohbot, V. D., Gupta, M., Banner, H., & Dahmani, L.(2011). Caudate nucleus-dependent response strategies in a virtual navigation task are associated with lower basal cortisol and impaired episodic memory. Neurobiology of Learning and Memory, 96(2), 173–180.
  • Bohbot, V. D., Lerch, J., Thorndycraft, B., Iaria, G., & Zijdenbos, A. P. (2007). Grey matter differences correlate with spontaneous strategies in a human virtual navigation task. The Journal of Neuroscience, 27(38), 10078–10083. https://doi.org/10.1523/JNEUROSCI.1763-07.2007
  • Boone, A. P., Gong, X., & Hegarty, M. (2018). Sex differences in navigation strategy and efficiency. Memory & Cognition, 46(6), 909–922. https://doi.org/10.3758/s13421-018-0811-y
  • Boone, A. P., Maghen, B., & Hegarty, M. (2019). Instructions matter: Individual and sex differences in navigation strategy and ability. Memory & Cognition.
  • Box, G. E., & Cox, D. R.(1964). An analysis of transformations. Journal of the Royal Statistical Society. Series B, Statistical Methodology, 26(2), 211–243.
  • Brown, T. I., Gagnon, S. A., & Wagner, A. D. (2020). Stress disrupts human hippocampal-prefrontal function during prospective spatial navigation and hinders flexible behavior. Current Biology, 30(10), 1821–1833. https://doi.org/10.1016/j.cub.2020.03.006
  • Brunyé, T. T., Wood, M. D., Houck, L. A., & Taylor, H. A. (2016). The path more traveled: Time pressure increases reliance on familiar route-based strategies during navigation. The Quarterly Journal of Experimental Psychology, 70(8), 1439–1452. https://doi.org/10.1080/17470218.2016.1187637
  • Bullock, T., & Giesbrecht, B. (2014). Acute exercise and aerobic fitness influence selective attention during visual search. Frontiers in Psychology, 5, 1290. https://doi.org/10.3389/fpsyg.2014.01290
  • Bullock, T., MacLean, M. H., Santander, T., Boone, A. P., Babenko, V., Dundon, N. M., Stuber, A., Jimmons, L., Raymer, J., Okafor, G. N., Miller, M. B., Giesbrecht, B., & Grafton, S. T. (2023). Habituation of the stress response multiplex to repeated cold pressor exposure. Frontiers in Physiology, 13, 2542. https://doi.org/10.3389/fphys.2022.752900
  • Credé, S., Thrash, T., Hölscher, C., & Fabrikant, S. I. (2019). The acquisition of survey knowledge for local and global landmark configurations under time pressure. Spatial Cognition and Computation, 19(3), 1–30. https://doi.org/10.1080/13875868.2019.1569016
  • de Quervain, D. J. F., Roozendaal, B., & McGaugh, J. L. (1998). Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature, 394(6695), 787–790. https://doi.org/10.1038/29542
  • de Quervain, D. J. F., Roozendaal, B., Nitsch, R. M., McGaugh, J. L., & Hock, C. (2000). Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nature Neuroscience, 3(4), 313–314. https://doi.org/10.1038/73873
  • Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130(3), 355–391. https://doi.org/10.1037/0033-2909.130.3.355
  • Dickerson, S. S., Mycek, P. J., & Zaldivar, F. (2008). Negative social evaluation, but not mere social presence, elicits cortisol responses to a laboratory stressor task. Health Psychology, 27(1), 116–121. https://doi.org/10.1037/0278-6133.27.1.116
  • Duncko, R., Cornwell, B., Cui, L., Merikangas, K. R., & Grillon, C. (2007). Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men. Learning & Memory, 14(5), 329–335. https://doi.org/10.1101/lm.483807
  • Furman, A. J., Clements-Stephens, A. M., Marchette, S. A., & Shelton, A. L. (2014). Persistent and stable biases in spatial learning mechanisms predict navigational style. Cognitive, Affective, & Behavioral Neuroscience, 14(4), 1375–1391. https://doi.org/10.3758/s13415-014-0279-6
  • Gagnon, S. A., & Wagner, A. D. (2016). Acute stress and episodic memory retrieval: neurobiological mechanisms and behavioral consequences. Annals of the New York Academy of Sciences, 1369(1), 55–75. https://doi.org/10.1111/nyas.12996
  • Hackney, A. C. (2006). Stress and the neuroendocrine system: The role of exercise as a stressor and modifier of stress. Expert Review of Endocrinology & Metabolism, 1(6), 783–792. https://doi.org/10.1586/17446651.1.6.783
  • Hegarty, M., He, C., Boone, A. P., Yu, S., Jacobs, E. G., & Chrastil, E. R. (2022). Understanding differences in wayfinding strategies. Topics in Cognitive Science, 15(1), 102–119. https://doi.org/10.1111/tops.12592
  • Hegarty, M., Montello, D. R., Richardson, A. E., Ishikawa, T., & Lovelace, K. (2006). Spatial abilities at different scales: Individual differences in aptitude-test performance and spatial-layout learning. Intelligence, 34(2), 151–176. https://doi.org/10.1016/j.intell.2005.09.005
  • Het, S., Ramlow, G., & Wolf, O. T. (2005). A meta-analytic review of the effects of acute cortisol administration on human memory. Psychoneuroendocrinology, 30(8), 771–784. https://doi.org/10.1016/j.psyneuen.2005.03.005
  • Het, S., Rohleder, N., Schoofs, D., Kirschbaum, C., & Wolf, O. T. (2009). Neuroendocrine and psychometric evaluation of a placebo version of the ‘trier social stress test’. Psychoneuroendocrinology, 34(7), 1075–1086. https://doi.org/10.1016/j.psyneuen.2009.02.008
  • Hines, E. A., & Brown, G. E. (1932). A standard stimulus for measuring vasomotor reactions: Its application in the study of hypertension. Proceedings of the Staff Meetings Mayo Clinic, 7, 332–335.
  • Iaria, G., Petrides, M., Dagher, A., Pike, B., & Bohbot, V. D. (2003). Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: Variability and change with practice. The Journal of Neuroscience, 23(13), 5945–5952. https://doi.org/10.1523/JNEUROSCI.23-13-05945.2003
  • Ishikawa, T., & Montello, D. R. (2006). Spatial knowledge acquisition from direct experience in the environment: Individual differences in the development of metric knowledge and the integration of separately learned places. Cognitive Psychology, 52(2), 93–129. https://doi.org/10.1016/j.cogpsych.2005.08.003
  • Kirschbaum, C., Pirke, K. M., & Hellhammer, D. H. (1993). The ‘trier social stress test’ – a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology, 28(1–2), 76–81. https://doi.org/10.1159/000119004
  • Kirschbaum, C., Wolf, O. T., May, M., Wippich, W., & Hellhammer, D. H. (1996). Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sciences, 58(17), 1475–1483. https://doi.org/10.1016/0024-3205(96)00118-X
  • Klopp, C., Garcia, C., Schulman, A. H., Ward, C. P., & Tartar, J. L. (2012). Acute social stress increases biochemical and self report markers of stress without altering spatial learning in humans. Activitas Nervosa Superior Rediviva, 33(4), 15–20.
  • Kozlowski, L. T., & Bryant, K. J. (1977). Sense of direction, spatial orientation, and cognitive maps. Journal of Experimental Psychology: Human Perception and Performance, 3(4), 590–598. https://doi.org/10.1037//0096-1523.3.4.590
  • Kumaran, D., & Maguire, E. A. (2005). The human hippocampus: Cognitive maps or relational memory? The Journal of Neuroscience, 25(31), 7254–7259. https://doi.org/10.1523/JNEUROSCI.1103-05.2005
  • Kumar, S., Iftekhar, A. S. M., Goebel, M., Bullock, T., MacLean, M. H., Miller, M. B., & Manjunath, B. S. (2021). StressNet: Detecting stress in thermal videos. Proceedings of the IEEE/CVF Winter Conference on Applications of Computer Vision (pp. 999–1009).
  • Lamotte, G., Boes, C. J., Low, P. A., & Coon, E. A. (2021). The expanding role of the cold pressor test: A brief history. Clinical Autonomic Research, 31(2), 153–155. https://doi.org/10.1007/s10286-021-00796-4
  • Larra, M. F., Schilling, T. M., Röhrig, P., & Schächinger, H. (2015). Enhanced stress response by a bilateral feet compared to a unilateral hand cold pressor test. Stress, 18(5), 589–596. https://doi.org/10.3109/10253890.2015.1053452
  • Lawton, C. A., Charleston, S. I., & Zieles, A. S. (1996). Individual-and gender-related differences in indoor wayfinding. Environment and Behavior, 28(2), 204–219. https://doi.org/10.1177/0013916596282003
  • Maguire, E. A., Burgess, N., Donnett, J. G., Frackowiak, R. S. J., Frith, C. D., & O’Keefe, J. (1998). Knowing where, and getting there: A human navigation network. Science, 280(5365), 921–924. https://doi.org/10.1126/science.280.5365.921
  • Maguire, E. A., Woollett, K., & Spiers, H. J. (2006). London taxi drivers and bus drivers: A structural MRI and neuro- psychological analysis. Hippocampus, 16(12), 1091–1101. https://doi.org/10.1002/hipo.20233
  • Marchette, S. A., Bakker, A., & Shelton, A. L. (2011). Cognitive mappers to creatures of habit: Differential engagement of place and response learning mechanisms predicts human navigational behavior. The Journal of Neuroscience, 31(43), 15264–15268. https://doi.org/10.1523/JNEUROSCI.3634-11.2011
  • McEwen, B. S., Weiss, J. M., & Schwartz, L. S. (1968). Selective retention of corticosterone by limbic structures in rat brain. Nature, 220(5170), 911–912. https://doi.org/10.1038/220911a0
  • Miller, R., & Plessow, F. (2013). Transformation techniques for cross-sectional and longitudinal endocrine data: Application to salivary cortisol concentrations. Psychoneuroendocrinology, 38(6), 941–946. https://doi.org/10.1016/j.psyneuen.2012.09.013
  • Montello, D. R. (2005). Navigation. In P. Shah & A. Miyake (Eds.), The Cambridge handbook of visuospatial thinking (pp. 257–294). Cambridge University Press.
  • Morey, R. D., & Rouder, J. N. (2022). BayesFactor: Computation of Bayes factors for common designs. R Package Version,0.9.12–.4.4. https://CRAN.R-project.org/package=BayesFactor
  • Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O’Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297(5868), 681–683. https://doi.org/10.1038/297681a0
  • O’Connor, P. J., & Corrigan, D. L. (1987). Influence of short-term cycling on salivary cortisol levels. Medicine and Science in Sports and Exercise, 19(3), 224–228. https://doi.org/10.1249/00005768-198706000-00007
  • O’Keefe, J., & Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Research, 34(1), 171–175. https://doi.org/10.1016/0006-8993(71)90358-1
  • O’Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Clarendon Press.
  • Packard, M. G., & McGaugh, J. L. (1996). Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory, 65(1), 65–72. https://doi.org/10.1006/nlme.1996.0007
  • Proffitt, D. R., Stefanucci, J., Banton, T., & Epstein, W. (2003). The role of effort in perceiving distance. Psychological Science, 14(2), 106–112. https://doi.org/10.1111/1467-9280.t01-1-01427
  • Pruessner, J. C., Dedovic, K., Khalili-Mahani, N., Engert, V., Pruessner, M., Buss, C. … Lupien, S. (2008). Deactivation of the limbic system during acute psychosocial stress: Evidence from positron emission tomography and functional magnetic resonance imaging studies. Biological Psychiatry, 63(2), 234–240. https://doi.org/10.1016/j.biopsych.2007.04.041
  • Richardson, A. E., & VanderKaay Tomasulo, M. M. (2011). Influence of acute stress on spatial tasks in humans. Physiology & Behavior, 103(5), 459–466. https://doi.org/10.1016/j.physbeh.2011.03.019
  • Richardson, A. E., & VanderKaay Tomasulo, M. M. (2022). Stress-induced HPA activation in virtual navigation and spatial attention performance. BMC Neuroscience, 23(1), 40. https://doi.org/10.1186/s12868-022-00722-y
  • Roig, M., Nordbrandt, S., Geertsen, S. S., & Nielsen, J. B. (2013). The effects of cardiovascular exercise on human memory: A review with meta-analysis. Neuroscience & Biobehavioral Reviews, 37(8), 1645–1666. https://doi.org/10.1016/j.neubiorev.2013.06.012
  • Schinazi, V. R., Nardi, D., Newcombe, N. S., Shipley, T. F., & Epstein, R. A. (2013). Hippocampal size predicts rapid learning of a cognitive map in humans. Hippocampus, 23(6), 515–528. https://doi.org/10.1002/hipo.22111
  • Schwabe, L., Oitzl, M. S., Philippsen, C., Richter, S., Bohringer, A., Wippich, W., & Schachinger, H. (2007). Stress modulates the use of spatial versus stimulus-response learning strategies in humans. Learning & Memory, 14(1–2), 109–116. https://doi.org/10.1101/lm.435807
  • Schwabe, L., & Wolf, O. T. (2013). Stress and multiple memory systems: From ‘thinking’ to ‘doing’. Trends in Cognitive Sciences, 17(2), 60–68. https://doi.org/10.1016/j.tics.2012.12.001
  • Segal, S. K., Cotman, C. W., & Cahill, L. F. (2012). Exercise-induced noradrenergic activation enhances memory consolidation in both normal aging and patients with amnestic mild cognitive impairment. Journal of Alzheimer’s Disease, 32(4), 1011–1018. https://doi.org/10.3233/JAD-2012-121078
  • Shields, G. S., Sazma, M. A., McCullough, A. M., & Yonelinas, A. P.(2017). The effects of acute stress on episodic memory: A meta-analysis and integrative review. Psychological Bulletin, 143(6), 636–675.
  • Smith, A. M., Floerke, V. A., & Thomas, A. K. (2016). Retrieval practice protects memory against acute stress. Science, 354(6315), 1046–1048. https://doi.org/10.1126/science.aah5067
  • Sutherland, R. J., Kolb, B., & Whishaw, I. Q. (1982). Spatial mapping: Definitive disruption by hippocampal or medial frontal cortical damage in the rat. Neuroscience Letters, 31(3), 271–276. https://doi.org/10.1016/0304-3940(82)90032-5
  • Thomas, K. G., Laurance, H. E., Nadel, L., & Jacobs, W. J. (2010). Stress-induced impairment of spatial navigation in females. South African Journal of Psychology, 40(1), 32–43. https://doi.org/10.1177/008124631004000104
  • van Gerven, D. J., Ferguson, T., & Skelton, R. W. (2016). Acute stress switches spatial navigation strategy from egocentric to allocentric in a virtual Morris water maze. Neurobiology of Learning and Memory, 132, 29–39. https://doi.org/10.1016/j.nlm.2016.05.003
  • Viru, A., & Viru, M. (2004). Cortisol-essential adaptation hormone in exercise. International Journal of Sports Medicine, 25(6), 461–464. https://doi.org/10.1055/s-2004-821068
  • Weisberg, S. M., & Newcombe, N. S. (2016). How do (some) people make a cognitive map? Routes, places, and working memory. Journal of Experimental Psychology: Learning, Memory, and Cognition, 42(5), 768–785. https://doi.org/10.1037/xlm0000200
  • Wiemers, U. S., Schoofs, D., & Wolf, O. T. (2013). A friendly version of the trier social stress test does not activate the HPA axis in healthy men and women. Stress, 16(2), 254–260. https://doi.org/10.3109/10253890.2012.714427

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.