Freedom of movement and the stability of its unfolding in free exploration of mice

Abstract

Exploration is a central component of human and animal behavior that has been studied in rodents for almost a century. The measures used by neuroscientists to characterize full-blown exploration are limited in exposing the dynamics of the exploratory process, leaving the morphogenesis of its structure and meaning hidden. By unfettering exploration from constraints imposed by hunger, thirst, coercion, and the confines of small cage and short session, using advanced computational tools, we reveal its meaning in the operational world of the mouse. Exploration consists of reiterated roundtrips of increasing amplitude and freedom, involving an increase in the number of independent dimensions along which the mouse moves (macro degrees of freedom). This measurable gradient can serve as a standard reference scale for the developmental dynamics of some aspects of the mouse's emotional-cognitive state and for the study of the interface between behavior and the neurophysiologic and genetic processes mediating it.

Fig. 1.

The moment-to-moment developmental sequence of free exploration. The developmental landmarks in a specific BALB/c mouse-session performed across a 3-h period. The spiral proceeding from top to bottom, first in the left and then in the right column, presents the time-series of 2-D locations on the path traced by the mouse. The enumerated figure-inserts show the 12 landmark motions described in the text, traced in red within the arena, and on the spiral. Blue dots indicate instances in which the mouse approached the cage doorway and did not enter the cage (cage-skips), or stopped short of returning all of the way home during a return (Home-related-shuttle). Absence of a blue dot implies departure into home-cage. Yellow path stands for the return portion within a Home-related-shuttle.

Fig. 2.

The generality of the developmental sequence in free BALB/c mice. Numerals and respective background colors represent the landmark motions that were described in Fig. 1 in the order of their emergence in each of the mice.

Fig. 3.

The build up of amplitude and complexity of movement in zero-, one-, and two-dimensions space in a free BALB/c mouse. (A) Build up in the portion of body area (in pixels) extending out of doorway during Peep-and-hide. (B1–4): The build up of angular positions (θ) across roundtrips (amplitude and complexity). Note change of time scale from (B1) through (B4). Black line, borderline movements. Blue data points, cage skips. Positive values designate right and negative values left borderline directions. Red lines, angular positions of doorway at ±360°. Graph lines between x-axis and red line represent full circles. All graphs start with the same initial roundtrip, progressively incorporating later roundtrips. (B5) Emergence and build up of radial movement away from wall (in green), superimposed on the θ plot (in black). Significant radial movements (incursions) are added only after 1.5 h.

Fig. 4.

The build up of amplitude and complexity of incursions. (A–D) Incursions are plotted side-by-side in the order of their performance, from the initial incursion to the incursion that reached the center, in a selected BALB/c mouse-session. For each incursion the x-axis demarcates the angular section (Δθ) it covers for that incursion along the wall, and the y-axis demarcates arena radius. Each of the graphs starts with the first Incursion and includes progressively later incursions. Black dots represent border-related shuttles. Cumulative paths of the respective incursions are plotted on the right of each graph. Numerals above circles represent the range of plotted incursions.

Fig. 5.

The generality of the developmental sequence in free C57BL/6 mice. Numerals and respective background colors represent the landmark motions that were described in Fig. 1 in the order of their emergence in each of the mice. Top two rows represent the prototype sequences of each of the two strains. Cross-the-doorway-and-retreat (Landmark 2) is skipped in all but one of the C57BL/6 mice; Extended-garden-roundtrips (4') are inserted in all C57BL/6 mice before or immediately after the onset of Borderline-roundtrips (6). Simple Incursions (9) typically emerge before the borderline dimension is exhausted (8) and early crossing of the center (11) occurs before Border-related-shuttles (10) in most of the mice.