Locomotor Response to Novelty: What Does It Tell Us?

Abstract

Individual differences in response strategies may be utilized to identify those at risk for the development of neuropsychiatric disorders such as depression, anxiety, and substance use. One behavioral attribute that has been used to predict later mood disorders and substance use disorders is an organism's predisposition for novelty-seeking, modeled in rodents as increased exploration of novel environments or stimuli. Despite documented correlations of locomotor response to a novel environment and disease-specific tendencies, it remains unclear whether the "response to novelty trait" is stable across time and environments. Adolescence is an important transitional time, associated with vulnerability for neuropsychiatric disorders. Only a few studies have assessed whether variations in novelty-seeking behaviors in adolescent animals translate to variations of susceptibility to neuropsychiatric disorders later in life, and it is unclear whether initial locomotor responses to novelty are stable across time and development. We examined whether locomotor response to a novel environment is a stable attribute across time in a series of Open Field tests in early adolescent (postnatal day [p] 23-25) late adolescent (p58-59) and adult (p72 and older) male Sprague-Dawley rats. We also examined the relation between the locomotor response to a novel environment and other measures of responding to novelty. Results suggest that locomotor response to a novel environment does not emerge as a stable behavioral attribute until late adolescence. They also suggest that locomotor response to a novel environment and novelty-seeking, as assessed with the Novelty Place Preference paradigm, capture nonoverlapping behavioral tendencies.

Keywords: adolescent; early experience; habituation; locomotion; rodent.

FIGURE 1

Experimental timeline. Age in postnatal days (p) for each test is indicated. Adult (n = 24) and early adolescent (n = 24) male rats were tested in the Open Field (OF) soon after arrival to the facility. Adults were given a second test 6 days later; a subset of adolescents (n = 12) were given a second test 1 day later.

FIGURE 2

Adult, but not early adolescent, locomotor activity in the Open Field is highly correlated over a long period of time. (A) Total distance traveled in response to a novel environment (Open Field, OF) of adult rats (n = 24, black circles) was highly correlated with total distance traveled in response to a novel environment 8 weeks after the initial OF test (r(22) = 0.75, p < 0.001). (B) Total distance traveled in response to a novel environment of early adolescent rats (n = 24, open squares) was not correlated with total distance traveled in response to a novel environment 5 weeks after the initial OF test (r(22) = 0.15, p > 0.05). Graphs show individual data points and regression lines for all rats exposed to each test.

FIGURE 3

Adult, but not early adolescent, locomotor activity in the Open Field is highly correlated over a short period of time. (A) Total distance traveled in response to a novel environment (Open Field, OF) of adult rats (n = 24, black circles) was highly correlated with total distance traveled in response to a novel environment 6 days after the initial OF test (r(22) = 0.89, p < 0.001). (B) Total distance traveled in response to a novel environment of early adolescent rats (n = 12, open squares) was not correlated 1 day after the initial OF test (r(10) = 0.36, p > 0.05). Graphs show individual data points and regression lines for all rats exposed to each test.

FIGURE 4

Late adolescent locomotor activity in the Open Field is highly correlated over a short period of time, and suggests a developmental component in the emergence of a stable trait. (A) Total distance traveled in response to a novel environment (Open Field, OF) of late adolescent rats (n = 10, gray squares) was highly correlated with total distance traveled in response to a novel environment 1 day after the initial OF test (r(8) = 0.79, p < 0.01). Graph shows individual data points and regression line for all 10 rats. (B) Total distance traveled in an initial Open Field test was ranked from lowest to highest, and divided into tertiles for adults, early adolescents, and late adolescents separately. For each age group, the top 1/3 of rats was classified as High Responders, the middle 1/3 of rats was classified as Mid Responders, and the bottom 1/3 of rats was classified as Low Responders. Graph shows the percentage of rats that maintained their initial classification in a later Open Field test 1 day (early adolescents, open bar; late adolescents, gray bar) or 6 days (adults, black bar) later.

FIGURE 5

Adult Low and High Responders have distinct locomotor activity profiles in the 2 h Open Field test. Distance traveled (cm) over time (summed in 5 min bins) for adult Low (solid line) and High Responders (dashed line) separately over the course of the 2 h Open Field test. Adults’ total distance traveled for the 2 h test was ranked from highest to lowest, and divided into tertiles; the bottom 1/3 of the distribution was classified as Low Responders (n = 8) and the top 1/3 of the distribution was classified as High Responders (n = 8). Activity of the middle 1/3 of the population (n = 8) is omitted for clarity. Values shown are group means of distance traveled over time, per 5 min bin ± SEMs.

FIGURE 6

Novelty Place Preference does not differ between Low and High Responders and does not correlate with locomotor response to novelty in the Open Field test. (A) Preference for a novel chamber in the Novelty Place Preference test was equivalent in adults classified as Low (dark slashes) and High Responders (gray slashes) from the 2 h Open Field test. Rats spent more time (s) in a novel chamber, compared to a small center chamber, or a chamber with which they had previously been exposed to (familiar chamber). Values shown are group means ± SEMs. (B) Total distance traveled (cm) in the Open Field test did not significantly correlate with preference for a novel chamber in the NPP (NPP % time novel), defined as: time spent in the novel chamber / (time spent in the novel + familiar chambers) (r(22) = 0.12, p > 0.05). (C) Rate of activity decline (cm/min) in the Open Field test also did not significantly correlate with preference for a novel chamber in the NPP (r(22) = 0.20, p > 0.05). Graphs show individual data points and regression line for all 24 rats; individual points are color‐coded for LR (black), mid (open), and HR (gray) classifications.