Towards a Characterization of Human Spatial Exploration Behavior

Overview

Journal Behav Res Methods

Publisher Springer

Date 2025 Jan 22

PMID 39843885

Authors

Valentin Baumann

Johannes Dambacher

Marit F L Ruitenberg

Judith Schomaker

Kerstin Krauel

Affiliations

Soon will be listed here.

Abstract

Spatial exploration is a complex behavior that can be used to gain information about developmental processes, personality traits, or mental disorders. Typically, this is done by analyzing movement throughout an unknown environment. However, in human research, until now there has been no overview on how to analyze movement trajectories with regard to exploration. In the current paper, we provide a discussion of the most common movement measures currently used in human research on spatial exploration, and suggest new indices to capture the efficiency of exploration. We additionally analyzed a large dataset (n = 409) of human participants exploring a novel virtual environment to investigate whether movement measures could be assigned to meaningful higher-order components. Hierarchical clustering of the different measures revealed three different components of exploration (exploratory behavior, spatial shape, and exploration efficiency) that in part replicate components of spatial exploratory behavior identified in animal studies. A validation of our analysis on a second dataset (n = 102) indicated that two of these clusters are stable across different contexts as well as participant samples. For the exploration efficiency cluster, our validation showed that it can be further differentiated into a goal-directed versus a general, area-directed component. By also sharing data and code for our analyses, our results provide much-needed tools for the systematic analysis of human spatial exploration behavior.

References

Kalueff A, Jensen C, Murphy D . Locomotory patterns, spatiotemporal organization of exploration and spatial memory in serotonin transporter knockout mice. Brain Res. 2007; 1169:87-97. DOI: 10.1016/j.brainres.2007.07.009. View

Brudzynski S, Krol S . Analysis of locomotor activity in the rat: parallelism index, a new measure of locomotor exploratory pattern. Physiol Behav. 1997; 62(3):635-42. DOI: 10.1016/s0031-9384(97)00189-3. View

Kakade S, Dayan P . Dopamine: generalization and bonuses. Neural Netw. 2002; 15(4-6):549-59. DOI: 10.1016/s0893-6080(02)00048-5. View

Paulus M, Geyer M, STERNBERG E . Differential movement patterns but not amount of activity in unconditioned motor behavior of Fischer, Lewis, and Sprague-Dawley rats. Physiol Behav. 1999; 65(3):601-6. DOI: 10.1016/s0031-9384(98)00195-4. View

Fulcher B, Little M, Jones N . Highly comparative time-series analysis: the empirical structure of time series and their methods. J R Soc Interface. 2013; 10(83):20130048. PMC: 3645413. DOI: 10.1098/rsif.2013.0048. View

Gottlieb J, Oudeyer P, Lopes M, Baranes A . Information-seeking, curiosity, and attention: computational and neural mechanisms. Trends Cogn Sci. 2013; 17(11):585-93. PMC: 4193662. DOI: 10.1016/j.tics.2013.09.001. View

Hejtmanek L, Starrett M, Ferrer E, Ekstrom A . How Much of What We Learn in Virtual Reality Transfers to Real-World Navigation?. Multisens Res. 2020; 33(4-5):479-503. DOI: 10.1163/22134808-20201445. View

Yaremych H, Kistler W, Trivedi N, Persky S . Path Tortuosity in Virtual Reality: A Novel Approach for Quantifying Behavioral Process in a Food Choice Context. Cyberpsychol Behav Soc Netw. 2019; 22(7):486-493. PMC: 6653789. DOI: 10.1089/cyber.2018.0644. View

Freund J, Brandmaier A, Lewejohann L, Kirste I, Kritzler M, Kruger A . Emergence of individuality in genetically identical mice. Science. 2013; 340(6133):756-9. DOI: 10.1126/science.1235294. View

10.

Johnson A, Varberg Z, Benhardus J, Maahs A, Schrater P . The hippocampus and exploration: dynamically evolving behavior and neural representations. Front Hum Neurosci. 2012; 6:216. PMC: 3404547. DOI: 10.3389/fnhum.2012.00216. View

11.

Young J, Minassian A, Paulus M, Geyer M, Perry W . A reverse-translational approach to bipolar disorder: rodent and human studies in the Behavioral Pattern Monitor. Neurosci Biobehav Rev. 2007; 31(6):882-96. PMC: 2025688. DOI: 10.1016/j.neubiorev.2007.05.009. View

12.

Mata R, Wilke A, Czienskowski U . Foraging across the life span: is there a reduction in exploration with aging?. Front Neurosci. 2013; 7:53. PMC: 3627975. DOI: 10.3389/fnins.2013.00053. View

13.

Batrancourt B, Lecouturier K, Ferrand-Verdejo J, Guillemot V, Azuar C, Bendetowicz D . Exploration Deficits Under Ecological Conditions as a Marker of Apathy in Frontotemporal Dementia. Front Neurol. 2019; 10:941. PMC: 6736613. DOI: 10.3389/fneur.2019.00941. View

14.

Markel A, Galaktionov I, Efimov V . [Factor analysis of rat behavior in the open-field test]. Zh Vyssh Nerv Deiat Im I P Pavlova. 1988; 38(5):855-63. View

15.

Reader S . Causes of Individual Differences in Animal Exploration and Search. Top Cogn Sci. 2015; 7(3):451-68. DOI: 10.1111/tops.12148. View

16.

Paulus M, Dulawa S, Ralph R, Geyer M . Behavioral organization is independent of locomotor activity in 129 and C57 mouse strains. Brain Res. 1999; 835(1):27-36. DOI: 10.1016/s0006-8993(99)01137-3. View

17.

Wolbers T, Hegarty M . What determines our navigational abilities?. Trends Cogn Sci. 2010; 14(3):138-46. DOI: 10.1016/j.tics.2010.01.001. View

18.

Schulz E, Wu C, Ruggeri A, Meder B . Searching for Rewards Like a Child Means Less Generalization and More Directed Exploration. Psychol Sci. 2019; 30(11):1561-1572. DOI: 10.1177/0956797619863663. View

19.

Schomaker J, Baumann V, Ruitenberg M . Effects of exploring a novel environment on memory across the lifespan. Sci Rep. 2022; 12(1):16631. PMC: 9533976. DOI: 10.1038/s41598-022-20562-4. View

20.

Clemenson G, Henningfield C, Stark C . Improving Hippocampal Memory Through the Experience of a Rich Minecraft Environment. Front Behav Neurosci. 2019; 13:57. PMC: 6437107. DOI: 10.3389/fnbeh.2019.00057. View