Comparative analysis of research behavior of laboratory mice and wild rodents in standard and enriched versions of the open field task

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Abstract

Exploratory activity is a vital form of behavior influenced by the habitat and individual experiences of animals. To assess the roles of these factors, we studied exploratory behavior in an identical setting among three rodent species that differ in their ecological niches, navigation characteristics, and levels of individual experience: wild animals from natural populations — bank voles (Clethrionomys glareolus) and the herb field mouse (Sylvaemus uralensis)—and C57BL/6J laboratory mice. Exploratory behavior was measure in a standardized open field test. To evaluate the influence of environmental novelty, animals had four sessions of empty open field exploration explored followed by four sessions in an enriched open field. Expert annotation of the behavioral patterns revealed that the animals engaged in 11 specific behavioral acts to explore the empty arena and 22 types of acts in the enriched arena. Notably, we identified specific behavioral acts in either wild rodents or laboratory mice. Bank voles displayed significantly less exploratory activity compared to the mouse species, which showed only slight differences in exploratory behavior. A key factor influencing the exploratory activity of the compared species was the enrichment of the arena with objects. The addition of objects not only increased the overall exploratory activity of the animals but also altered the structure of their exploratory behavior. Contrary to the initial hypothesis, the factor of environmental novelty had the least influence on behavior, with effects varying depending on specific behavioral forms and manifesting only in combination with other factors. The results reveal complex and nonlinear relationships among the factors determining rodent behavior in the open field task, which should be considered in analyzing the neural bases of this behavior and interpreting exploratory behavior in natural conditions.

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About the authors

G. A. Rogov

Lomonosov Moscow State University

Author for correspondence.
Email: oivashkina@gmail.com
Russian Federation, Moscow

K. A. Toropova

Lomonosov Moscow State University

Email: oivashkina@gmail.com
Russian Federation, Moscow

O. S. Rogozhnikova

Lomonosov Moscow State University

Email: oivashkina@gmail.com
Russian Federation, Moscow

V. Yu. Oleynichenko

Lomonosov Moscow State University

Email: oivashkina@gmail.com
Russian Federation, Moscow

O. I. Ivashkina

Lomonosov Moscow State University

Email: oivashkina@gmail.com
Russian Federation, Moscow

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Supplementary files

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2. Fig. 1. The scheme of the experiment. (a) – empty open field, (б) – enriched open field, (в) – photo of enriched open field, (г) – experimental procedure.

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3. Fig. 2. The number and total duration of sniffing and head raises in bank voles (C. glareolus), herb field mice (S. uralensis), and laboratory mice (C57Bl/6J) in the empty and enriched open field (OF). (a) – number of sniffing, (б) – total duration of sniffing, (в) – number of head raises, (г) – total duration of head raises. B-1, B-4 – first and fourth sections in the empty OF, respectively; C-1, C-4 – first and fourth sections in the enriched OF, respectively. *** – p < 0.0001, factor “type of OF,” in the empty OF, animals exhibit more sniffing, more head raises, and greater total duration of head raises compared to the enriched OF; xx – p < 0.01, factor “type of OF,” in the enriched OF, the total duration of sniffing is greater than in the empty OF; ++ – p < 0.01, +++ – p < 0.0001 in pairwise comparisons of each species with each other; ~~ – p < 0.01 when comparing bank voles and laboratory mice with herb field mice; ### – p < 0.0001 when comparing bank voles and small forest mice with laboratory mice, Tukey’s post hoc test.

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4. Fig. 3. The number and total duration of supported and unsupported rearing in bank voles (C. glareolus), herb field mice (S. uralensis), and laboratory mice (C57Bl/6J) in empty and enriched OF. (a) – number of supported rearings, (б) – total duration of supported rearings, (в) – number of unsupported rearings, (г) – total duration of unsupported rearings. B-1, B-4 – first and fourth exposure to the empty OF, respectively; C-1, C-4 – first and fourth exposure to the enriched OF, respectively. * – p < 0.05, *** – p < 0.0001, factor “type of OF”, animals in the empty OF perform more supported and unsupported rearings, and the total duration of supported rearings is higher than in the enriched OF; +++ – p < 0.0001 in pairwise comparison between each species; ^^^ – p < 0.0001 when comparing herb field mice and laboratory mice with bank voles; @@ – p = 0.009 in comparison of the duration of unsupported rearings in laboratory mice during the 1st and 4th exposure to the enriched OF, Tukey’s post hoc test.

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5. Fig. 4. The number of object exploration acts in bank voles (C. glareolus), herb field mice (S. uralensis), and laboratory mice (C57Bl/6J) in the enriched OF. (a) – number of object sniffings, (б) – number of object touches, (в) – number of instances of being on the object, (г) – number of crossings over objects. C-1, C-4 – first and fourth exposure to the enriched OF. ** – p < 0.01, *** – p < 0.0001, factor “day,” animals perform more sniffing and touching of objects during the 1st exposure to the enriched OF than during the 4th exposure; +++ – p < 0.0001 in pairwise comparison between each species during the 1st exposure to the enriched OF; ### – p < 0.0001 when comparing bank voles and herb field mice with laboratory mice; ^ – p < 0.05 when comparing herb field mice with bank voles, Tukey’s post hoc test.

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6. Fig. 5. The proportion of bank voles (C. glareolus), herb field mice (S. uralensis), and laboratory mice (C57Bl/6J) demonstrating jumping (a), resting (б), and scratching (в) in the empty and enriched OF. ** – p < 0.0056 when comparing the empty OF with the enriched OF; ^ – p < 0.0056 when comparing herb field mice and laboratory mice with bank voles; # – p < 0.0056 when comparing bank voles and herb field mice with laboratory mice; @ – p < 0.0056 when comparing the proportion of laboratory mice performing jumps in the empty and enriched OF, chi-square test.

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