“It’s all in their head”: hierarchical exploration of a three-dimensional layered pyramid in rats

Abstract

Wayfinding in a three-dimensional (3D) environment is intricate, and surface-bounded animals may overcome this complexity by breaking it down into horizontal layers along with the vertical location of each layer. Here, we examined how rats explored a layered pyramid placed in a large open field. We found that exploration presented a hierarchical (or fractal) shape of three types of roundtrips: (1) from the primary home-base to the open-field floor; (2) from the floor up and down the pyramid levels; and (3) from local home-base on each pyramid level. Ascent was slow and interrupted, whereas descent was fast. This difference was a result of level altitude, remaining after data were normalized proportionally to level area. In contrast, the time spent and the distance traveled on each level were dependent on level area, not on level altitude. This structure of spatial behavior accords with multilevel exploration, presenting a relatively independent exploration of each level. The vertical dimension in this experiment thus did not alter the typical spatiotemporal behavior, and the 3D environment was explored by application of the same spatiotemporal approach as that of a horizontal open field. We suggest that this lack of alteration is due to the horizontal posture of the animal’s head and trunk during progression on the pyramid. This behavior also seems to fit the bicoding hypothesis, in which the vertical information is virtually contextual (non-metric), and so, when the rat progresses to a new level, it explores it as a newly accessed horizontal floor area.

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References

  1. Avni R, Tzvaigrach Y, Eilam D (2008) Exploration and navigation in the blind mole rat (Spalax ehrenbergi): global calibration as a primer of spatial representation. J Exp Biol 211:2817–2826

    Article  Google Scholar 

  2. Berthoza A, Thibaultb G (2013) Learning landmarks and routes in multifloored buildings. Behav Brain Sci 36:545

    Article  Google Scholar 

  3. Calori C (2007) Signage and wayfinding design: a complete guide to creating environmental graphic design systems. John Wiley and Sons, Hoboken

    Google Scholar 

  4. Drai D, Golani I (2001) SEE: a tool for the visualization and analysis of rodent exploratory behavior. Neurosci Biobehav Rev 25:409–426

    CAS  Article  Google Scholar 

  5. Eilam D (2014) Of mice and men: building blocks in cognitive mapping. Neurosci Biobehav Rev 47:393–409

    Article  Google Scholar 

  6. Eilam D, Golani I (1989) Home base behavior of rats (Rattus norvegicus) exploring a novel environment. Behav Brain Res 34:199–211

    CAS  Article  Google Scholar 

  7. Finkelstein A, Derdikman D, Rubin A, Foerster JN, Las L, Ulanovsky N (2015) Three-dimensional head-direction coding in the bat brain. Nature 517:159–164

    CAS  Article  Google Scholar 

  8. Golani I, Benjamini Y, Eilam D (1993) Stopping Behavior—constraints on exploration in rats (Rattus norvegicus). Behav Brain Res 53:21–33

    CAS  Article  Google Scholar 

  9. Grobéty MC, Schenk F (1992) The influence of spatial irregularity upon radial-maze performance in the rat. Lern Behav 20:393–400

    Article  Google Scholar 

  10. Hao J, Ching Chiuan Y (2009) Wayfinding in complex multi-storey buildings: a vision-simulation-augmented wayfinding protocol study. Paper presented at the Undisciplined! Design Research Society Conference, Sheffield

  11. Hayman R, Verriotis MA, Jovalekic A, Fenton AA, Jeffery KA (2011) Anisotropic encoding of three-dimensional space by place cells and grid cells. Nat Neurosci 14:1182–1188

    CAS  Article  Google Scholar 

  12. Hen I, Sakov A, Kafkafi N, Golani I, Benjamini Y (2004) The dynamics of spatial behavior: how can robust smoothing techniques help? J Neuroscience Meth 133:161–172

    Article  Google Scholar 

  13. Hines DJ, Whishaw IQ (2005) Home bases formed to visual cues but not to self-movement (dead reckoning) cues in exploring hippocampectomized rats. Eur J Neurosci 22:2363–2375

    Article  Google Scholar 

  14. Holbrook RI, Burt de Perera T (2009) Separate encoding of vertical and horizontal components of space during orientation in fish. Anim Behav 78:241–245

    Article  Google Scholar 

  15. Hölscher C, Meilinger T, Vrachliotis G, Brösamle M, Knauff M (2006) Up the down staircase: wayfinding strategies in multi-level buildings. J Environ Psychol 26:284–299

    Article  Google Scholar 

  16. Hölscher C, Brösamle M, Vrachliotis G (2012) Challenges in multilevel wayfinding: a case study with the space syntax technique. Environ Plan B 39:63–82

    Article  Google Scholar 

  17. Jeffery KA, Jovalekic A, Verriotis MA, Hayman R (2013) Navigating in a three-dimensional world. Behav Brain Sci 36:523–587

    Article  Google Scholar 

  18. Jeffery KJ, Wilson JJ, Casali G, Hayman RM (2015) Neural encoding of large-scale three-dimensional space—properties and constraints. Front Psychol 6:927

    Article  Google Scholar 

  19. Jovalekic A, Hayman R, Becares N, Reid H, Thomas G, Wilson J, Jeffery K (2011) Horizontal biases in rats’ use of three-dimensional space. Behav Brain Res 222:279–288

    Article  Google Scholar 

  20. Montello DR, Pick HL (1993) Integrating knowledge of vertically aligned largescale spaces. Environ Behav 25:457–484

    Article  Google Scholar 

  21. Page HJI, Wilson JJ, Jeffery KA (2018) A dual-axis rotation rule for updating the head direction cell reference frame during movement in three dimensions. J Neurophysiol 119:192–208

    Article  Google Scholar 

  22. Rozenfeld HD, Makse HA (2009) Fractality and the percolation transition in complex networks. Chem Eng Sci 64:4572–4575

    CAS  Article  Google Scholar 

  23. Rozenfeld HD, Rybski D, Andrade JSJ, Batty M, Stanley HE, Makse HA (2008) Laws of population growth. Proc Nat Acad Sci USA 105:18702–18707

    CAS  Article  Google Scholar 

  24. Sakov A, Golani I, Lipkind D, Benjamini Y (2010) High-throughput data analysis in behavior genetics. Ann Appl Stat 4:743–763

    Article  Google Scholar 

  25. Scatà G, Jozet-Alves C, Thomasse C, Josef N, Shashar N (2016) Spatial learning in the cuttlefish Sepia officinalis: preference for vertical over horizontal information. J Exp Biol 219:2928–2933

    Article  Google Scholar 

  26. Scatà G, Darmaillacq AS, Dickel L, McCusker S, Shashar N (2017) Going up or sideways? Perception of space and obstacles negotiating by cuttlefish. Front Physiol 8:173

    Article  Google Scholar 

  27. Shinder ME, Taube JS (2019) Three-dimensional tuning of head direction cells in rats. J Neurophysiol 121:4–37

    Article  Google Scholar 

  28. Taube JS (2011) Head direction cell firing properties and behavioural performance in 3-D space. J Physiol 589:835–841

    CAS  Article  Google Scholar 

  29. Tchernichovski O, Benjamini Y, Golani I (1998) The dynamics of long-term exploration in the rat. Part 1. A phase-plane analysis of the relationship between location and velocity. Biol Cyber 78:423–432

    CAS  Article  Google Scholar 

  30. Tenbrink T, Bergmann E, Konieczny L (2011) Wayfinding and description strategies in an unfamiliar complex building. Proc Ann Meet Cogn Sci Soc 33:1262–1267

    Google Scholar 

  31. Valerio S, Clark BJ, Chan JHM, Frost CP, Harris MJ, Taube JS (2010) Directional learning, but no spatial mapping by rats performing a navigational task in an inverted orientation. Neurobio Learn Mem 93:495–505

    Article  Google Scholar 

  32. Walsh RN, Cummins RA (1976) The open field test: a critical review. Psychol Bull 83:482–504

    CAS  Article  Google Scholar 

  33. Weisberg SM, Newcombe S (2013) Are all types of vertical information created equal? Behav Brain Sci 36:568–569

    Article  Google Scholar 

  34. Weiss S, Yaski O, Eilam D, Portugali J, Blumenfeld-Lieberthal E (2012) Network analysis of rat spatial cognition: behaviorally-established symmetry in a physically asymmetrical environment. PLoS One 7:e40760

    CAS  Article  Google Scholar 

  35. Wexler Y, Benjamini Y, Golani I (2018) Vertical exploration and dimensional modularity in mice. Roy Soc Open Sci 5:180069

    Article  Google Scholar 

  36. Wilson P, Foreman N, Stanton D, Duffy H (2004) Memory for targets in a multilevel simulated environment: evidence for vertical asymmetry in spatial memory. Mem Cogn 32:283–297

    Article  Google Scholar 

  37. Wolf S, Roper M, Chittka L (2015) Bumblebees utilize floral cues differently on vertically and horizontally arranged flowers. Behav Ecol 26:773–781

    Article  Google Scholar 

  38. Yaski O, Eilam D (2007) The impact of landmark properties in shaping exploration and navigation. Anim Cogn 10:415–428

    Article  Google Scholar 

  39. Yasumuroa H, Ikeda Y (2018) Environmental enrichment affects the ontogeny of learning, memory, and depth perception of the pharaoh cuttlefish Sepia pharaonis. Zoology 128:27–37

    Article  Google Scholar 

  40. Yoder RM, Taube JS (2014) The vestibular contribution to the head direction signal and navigation. Front Integr Neurosci 8:32

    Article  Google Scholar 

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Acknowledgements

This study is dedicated to the memory of Daniel Serruya, who was my first graduate student 30 years ago. Daniel, who published his study on the rock hyrax in 1996, was not only my student, but also became a much loved family friend (DE). We are grateful to Ms. Pazit Zadicario and Roi Gerstel for their help in testing and in data acquisition and analysis, and to Ms. Naomi Paz for language editing. The study was supported by a TAU Vice-President’s internal grant for research encouragement # 0604313192 to DE.

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Correspondence to David Eilam.

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The experiments and maintenance conditions for the rats were carried out under the regulations and approval of the Institutional Committee for Animal Experimentation at Tel-Aviv University (permit 04-19-009).

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Appendix

Appendix

Normalized data in ascending compared to descending the pyramid levels

Data were normalized by taking the area of the first level as one unit, and adjusting the time spent or distance traveled on each level according to the proportion between the area of that level and the area of the first level. For the normalized time spent on a level before ascent and descent, a two-way repeated-measure ANOVA revealed that there was no significant difference between levels (F3,36 = 0.22; p > 0.05). There was a significant difference between time spent on a level when ascending and the time spent on the same level when descending (F1,36 = 6.65; p = 0.014). There was also an interaction between the time on level and ascent/descent time (F3,36 = 3.11; p = 0.040). For the normalized data of the distance traveled on the levels before ascending vs. before descending, a two-way repeated-measure ANOVA revealed no significant effect between distance traveled on the levels (F3,36 = 1.48; p > 0.05), but a significant difference between the distance traveled in ascending compared to descending (F1,36 = 14.6; p = 0.0005), and an interaction between distance traveled on a level and distance traveled in ascending vs. descending (F3,36 = 4.35; p = 0.0103) (see Tables 1 and 2).

Table 1 Normalized data for the time spent and distance traveled on the pyramid levels
Table 2 Home-base on the floor compared to home-base on the pyramid levels

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Hagbi, Z., Dorfman, A., Blumenfeld-Lieberthal, E. et al. “It’s all in their head”: hierarchical exploration of a three-dimensional layered pyramid in rats. Anim Cogn 23, 277–288 (2020). https://doi.org/10.1007/s10071-019-01332-8

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Keywords

  • Roundtrip
  • Exploration
  • Open field
  • Multilevel
  • Bicoding
  • Quasiplanar model