Skip to main content

Human place and response learning: navigation strategy selection, pupil size and gaze behavior

Abstract

In this study, we examined the cognitive processes and ocular behavior associated with on-going navigation strategy choice using a route learning paradigm that distinguishes between three different wayfinding strategies: an allocentric place strategy, and the egocentric associative cue and beacon response strategies. Participants approached intersections of a known route from a variety of directions, and were asked to indicate the direction in which the original route continued. Their responses in a subset of these test trials allowed the assessment of strategy choice over the course of six experimental blocks. The behavioral data revealed an initial maladaptive bias for a beacon response strategy, with shifts in favor of the optimal configuration place strategy occurring over the course of the experiment. Response time analysis suggests that the configuration strategy relied on spatial transformations applied to a viewpoint-dependent spatial representation, rather than direct access to an allocentric representation. Furthermore, pupillary measures reflected the employment of place and response strategies throughout the experiment, with increasing use of the more cognitively demanding configuration strategy associated with increases in pupil dilation. During test trials in which known intersections were approached from different directions, visual attention was directed to the landmark encoded during learning as well as the intended movement direction. Interestingly, the encoded landmark did not differ between the three navigation strategies, which is discussed in the context of initial strategy choice and the parallel acquisition of place and response knowledge.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Notes

  1. Use of the configuration strategy throughout the experiment will result in 100 % performance, use of the beacon strategy will result in 66.66 % performance (only incorrect when the approach direction at test differs from training by 90°), and use of the associative cue strategy will result in 33.33 % performance (only correct during same-direction trials).

  2. While a ‘move towards’ rule is typically associated with the beacon strategy (Waller & Lippa, 2007), we believe beacon users adopt a ‘turn towards’ rule in this paradigm. As each landmark at an intersection adjoins two intersection pathways, use of a ‘move towards’ rule at selected same-direction trials can be satisfied by correctly turning towards the beacon or by incorrectly continuing straight ahead, while use of a configuration, associative cue or ‘turn towards’ beacon strategy would result in the correct answer. A straight ahead response was made in only 5.29 % of these trials, strongly suggesting beacon users employed a ‘turn towards’ rule.

  3. It should be noted that we assume the configuration, associative cue and beacon strategies encode the route congruent landmark during learning. If this is not the case, the predictions by all three models will be incorrect.

References

  • Andersen, N. E., Dahmani, L., Konishi, K., & Bohbot, V. D. (2012). Eye tracking, strategies, and sex differences in virtual navigation. Neurobiology of Learning and Memory, 97(1), 81–89.

    PubMed  Article  Google Scholar 

  • Beatty, J. (1982). Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychological Bulletin, 91(2), 276–292.

    PubMed  Article  Google Scholar 

  • Boksem, M. A., Meijman, T. F., & Lorist, M. M. (2005). Effects of mental fatigue on attention: an ERP study. Cognitive Brain Research, 25(1), 107–116.

    PubMed  Article  Google Scholar 

  • Cassel, R., Kelche, C., Lecourtier, L., & Cassel, J.-C. (2012). The match/mismatch of visuo-spatial cues between acquisition and retrieval contexts influences the expression of response vs. place memory in rats. Behavioural Brain Research, 230(2), 333–342.

    PubMed  Article  Google Scholar 

  • Diwadkar, V. A., & McNamara, T. P. (1997). Viewpoint dependence in scene recognition. Psychological Science, 8(4), 302–307.

    Article  Google Scholar 

  • Grasso, R., Prévost, P., Ivanenko, Y. P., & Berthoz, A. (1998). Eye-head coordination for the steering of locomotion in humans: an anticipatory synergy. Neuroscience Letters, 253(2), 115–118.

    PubMed  Article  Google Scholar 

  • Hamilton, D. A., Driscoll, I., & Sutherland, R. J. (2002). Human place learning in a virtual Morris water task: some important constraints on the flexibility of place navigation. Behavioural Brain Research, 129, 159–170.

    PubMed  Article  Google Scholar 

  • Hartley, T., Maguire, E. A., Spiers, H. J., & Burgess, N. (2003). The well-worn route and the path less travelled: distinct neural bases of route following and wayfinding in humans. Neuron, 37(5), 877–888.

    PubMed  Article  Google Scholar 

  • Hegarty, M., & Waller, D. (2004). A dissociation between mental rotation and perspective-taking spatial abilities. Intelligence, 32(2), 175–191.

    Article  Google Scholar 

  • Hess, E. H., & Polt, J. M. (1964). Pupil size in relation to mental activity during simple problem-solving. Science, 143, 1190–1192.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Iglói, K., Zaoui, M., Berthoz, A., & Rondi-Reig, L. (2009). Sequential egocentric strategy is acquired as early as allocentric strategy: Parallel acquisition of these two navigation strategies. Hippocampus, 19(12), 1199–1211.

    PubMed  Article  Google Scholar 

  • Just, M. A., & Carpenter, P. A. (1993). The intensity dimension of thought: pupillometric indices of sentence processing. Canadian Journal of Experimental Psychology, 47(2), 310–339.

    PubMed  Article  Google Scholar 

  • Kahneman, D., & Beatty, J. (1966). Pupil diameter and load on memory. Science, 154(3756), 1583–1585.

    PubMed  Article  Google Scholar 

  • King, J. A., Burgess, N., Hartley, T., Vargha-Khadem, F., & O’Keefe, J. (2002). Human hippocampus and viewpoint dependence in spatial memory. Hippocampus, 12(6), 811–820.

    PubMed  Article  Google Scholar 

  • Kozhevnikov, M., Motes, M. A., Rasch, B., & Blajenkova, O. (2006). Perspective-taking vs. mental rotation transformations and how they predict spatial navigation performance. Applied Cognitive Psychology, 20(3), 397–417.

    Article  Google Scholar 

  • Livingstone-Lee, S. A., Murchison, S., Zeman, P. M., Ghandi, M., van Gerven, D., Stewart, L., et al. (2011). Simple gaze analysis and special design of a virtual Morris water maze provides a new method for differentiating egocentric and allocentric navigation strategy choice. Behavioural Brain Research, 225(1), 117–125.

    PubMed  Article  Google Scholar 

  • Lowenstein, O., Feinberg, R., & Loewenfeld, I. E. (1963). Pupillary movements during acute and chronic fatigue. Investigative Ophthalmology & Visual Science, 2(2), 138–157.

    Google Scholar 

  • Manor, B. R., & Gordon, E. (2003). Defining the temporal threshold for ocular fixation in free-viewing visuocognitive tasks. Journal of Neuroscience Methods, 128(1), 85–93.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • Marshall, S. P., Pleydell-Pearce, C. W., & Dickson, B. T. (2003). Integrating psychophysiological measures of cognitive workload and eye movements to detect strategy shifts. In Proceedings of the 36th annual Hawaii international conference on System Sciences. Hawaii: IEEE.

  • Matthews, G., & Desmond, P. A. (2002). Task-induced fatigue states and simulated driving performance. The Quarterly Journal of Experimental Psychology: Section A, 55(2), 659–686.

    Article  Google Scholar 

  • Mueller, S. C., Jackson, C. P. T., & Skelton, R. W. (2008). Sex differences in a virtual water maze: an eye tracking and pupillometry study. Behavioural Brain Research, 193(2), 209–215.

    PubMed  Article  Google Scholar 

  • Nishiyama, J., Tanida, K., Kusumi, M., & Hirata, Y. (2007). The pupil as a possible premonitor of drowsiness. In Proceedings of the 29th annual international conference of the IEEE Engineering in Medicine and Biology Society. Lyon: IEEE.

  • O’Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Oxford University Press.

    Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • Schmitzer-Torbert, N. (2007). Place and response learning in human virtual navigation: Behavioral measures and gender differences. Behavioral Neuroscience, 121(2), 277–290.

    PubMed  Article  Google Scholar 

  • Shelton, A. L., & McNamara, T. P. (2001). Systems of spatial reference in human memory. Cognitive Psychology, 43(4), 274–310.

    PubMed  Article  Google Scholar 

  • Sibley, C., Coyne, J., & Baldwin, C. (2011). Pupil dilation as an index of learning. In Proceedings of the Human Factors and Ergonomics Society 55th Annual Meeting. Las Vegas: Sage.

  • Siegel, A. W., & White, S. H. (1975). The development of spatial representations of large-scale environments. In H. W. Reese (Ed.), Advances in child development and behaviour (Vol. 10, pp. 9–55). New York: Academic Press.

    Google Scholar 

  • Tlauka, M., & Wilson, P. N. (1994). The effect of landmarks on route-learning in a computer-simulated environment. Journal of Environmental Psychology, 14(4), 305–313.

    Article  Google Scholar 

  • Tolman, E. C. (1948). Cognitive maps in rats and men. Psychological Review, 55(4), 189–208.

    PubMed  Article  Google Scholar 

  • Waller, D., & Lippa, Y. (2007). Landmarks as beacons and associative cues: their role in route learning. Memory and Cognition, 35(5), 910–924.

    PubMed  Article  Google Scholar 

  • Wang, R. F., & Spelke, E. S. (2002). Human spatial representation: insights from animals. Trends in Cognitive Sciences, 6(9), 376–382.

    PubMed  Article  Google Scholar 

  • Wiener, J. M., de Condappa, O., Harris, M. A., & Wolbers, T. (2013). Maladaptive bias for extrahippocampal navigation strategies in aging humans. The Journal of Neuroscience, 33(14), 6012–6017.

    PubMed  Article  Google Scholar 

  • Wiener, J. M., de Condappa, O., & Höelscher, C. (2011). Do you have to look where you go? Gaze behaviour during spatial decision making. In L. Carlson, C. Höelscher, & T. F. Shipley (Eds.), Proceedings of the 33rd Annual Conference of the Cognitive Science Society. Austin: Cognitive Science Society.

    Google Scholar 

  • Wiener, J. M., Höelscher, C., Büchner, S., & Konieczny, L. (2012). Gaze behaviour during space perception and spatial decision making. Psychological Research, 76(6), 713–729.

    PubMed  Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Olivier de Condappa.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

de Condappa, O., Wiener, J.M. Human place and response learning: navigation strategy selection, pupil size and gaze behavior. Psychological Research 80, 82–93 (2016). https://doi.org/10.1007/s00426-014-0642-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00426-014-0642-9

Keywords

  • Test Trial
  • Experimental Block
  • Pupil Dilation
  • Response Strategy
  • Pupil Size