In order to directly assess the possibility that differential rates of habituation between fast and slow learners underlies the relationship between general learning abilities and exploration, it was necessary to equalize rates of habituation in fast and slow learners and to observe the resultant effect on the correlation between exploration and general learning performance. To this end, we observed the stability of the relationship between exploratory measures and general learning abilities under two different habituation conditions in two independent tasks. We hypothesized that when levels of habituation varied across individual mice (owing to differences in general learning ability), those variable levels of habituation would have commensurate effects on related exploratory behaviors. For instance, animals that habituate to the walled portions of a novel open field faster (i.e., learn faster) would be more prone to explore the unwalled portions of the field earlier in a bout of exploration. This could account for the common observation of a robust relationship between general learning abilities and measures of exploration in the open field. In contrast, if rates of habituation mediate the relationship between general learning abilities and exploration, when exploration is assessed at a point at which habituation is equal between fast and slow learners (e.g., later in a period of exposure to a novel field), the correlation between general learning performance and exploration should be attenuated. This can be thought of as a sequence of influences, where variability in general learning abilities influences habituation rates, which in turn influences variability in exploration. In this manner, eliminating variability in habituation would disrupt this chain of influences and would eliminate the relationship between general learning abilities and exploration.
Normalizing the level of habituation across animals can be achieved in one of two ways. First, all animals can be allowed to reach the similar asymptotic levels of habituation. In this manner individuals would presumably reach a habituative ceiling, thereby eliminating variability in habituation levels between mice and hence its effect on exploratory behaviors. Alternatively, exploratory behaviors can be measured when animals reach a specified level of habituation (i.e., reach a habituative criterion), regardless of how long it takes individuals to reach that level.
To achieve the first method of reducing variability in habituation levels, we administered an open field test which is substantially longer (12 min) than that used to observe a correlation between general learning ability and exploration in the field (i.e., 4 min). While a direct measure of habituation can not be obtained in this task, animals would presumably vary in the degree to which they would have habituated to the novel field early in a bout of exploration (e.g., at 4 min) relative to later in a bout of exploration (e.g., at 12 min). Thus we might anticipate that exploratory behavior during the first 4 min of a 12 min bout would better predict general learning performance than exploratory behavior in the last 4 min of a 12 min bout.
To achieve the second method of equating the level of habituation across individual animals, a nose poke exploration task was used. Here, animals explored two objects, across multiple sessions, by nose poking through a hole board. In the test session, one of the two objects was switched and exploration of the novel object was assessed. The level of habituation reached was left incomplete, although comparable levels were attained for all animals. This was accomplished by administering the critical test (i.e., replacement of one of two objects) after a number of training sessions which was known (based on pilot data) to produce incomplete levels of habituation. In addition, to eliminate variability (between animals) in habituation levels at the time of testing, animals were exposed to the test object after the same level of habituation (a pre-determined criterion) to the familiar objects was reached by each individual animal.
If differential rates of habituation (between animals of high or low general learning ability) underlie the relationship between general learning abilities and exploration, the relationship should be observed when levels of habituation are left variable across animals (i.e., during early time points in the open field or in initial exploration of a novel object) but should be eliminated when levels of habituation are more complete or are held constant across animals (i.e., during late time points in the open field or nose poke exploration assessed after all animals had reached a comparable habituation criterion).
Twenty-four outbred CD-1 mice were obtained from Harlan Sprague Dawley, Inc. at 45 days of age and participated in both the open field and novel object exploration tests. For the open field experiment, 23 additional animals (for a total of 47 in the open field) were added to the analysis (these animals became available from an experiment that was being concurrently performed). Animals were acclimated to our laboratory until 62 days of age, during which time they were handled for 90 sec/day, 5 days/week. This handling insured that differential stress responses to the experimenters, and any associated effects on learning, were minimized. Animals were individually housed in clear boxes with floors lined with wood shavings in a humidity- and temperature-controlled vivarium adjacent to testing rooms. A 12hr/12hr light/dark cycle was maintained. All manipulations and testing occurred around the middle portion of the light cycle.
3.2.2. Apparatus and Procedure 18.104.22.168. Learning Battery
The order of testing was intended to provide a temporal separation between any two tasks that were motivated by either food or water deprivation (to minimize excessive physical strain and to mitigate potential cross-task influences due to motivational factors). In addition, the testing order was designed to separate tasks based on similar processes or motor requirements (e.g., mazes of a similar nature, activity vs. passivity). All animals were tested in the following order: Lashley maze, passive avoidance, odor discrimination, fear conditioning, water maze.
22.214.171.124.1. Lashley III Maze
The Lashley III maze consisted of a start box, four interconnected alleys, and a goal box containing a food reward. The maze was scaled for mice, and parameters were developed that supported rapid acquisition. Over trials, the latency of mice to locate the goal box decreased, as did their errors (i.e., wrong turns or retracing). The maze was constructed of black Plexiglas. A 2 cm wide x 0.1 cm deep white cup was located in the rear portion of the goal box, and 45 mg BioServe (rodent grain) pellets served as reinforcers. Illumination was 80 lux at the floor of the maze. The maze was isolated behind a shield of white Plexiglas to prevent the use of extra-maze landmark cues.
Food-deprived animals were acclimated and trained on two successive days. On the day prior to acclimation, when ad libitum food was removed near the end of the light cycle, all animals were provided with two food pellets in their home cages to familiarize them with the novel reinforcer. On the acclimation day, each mouse was placed in the four alleys of the maze, but the openings between the alleys were blocked so that the animals could not navigate the maze. Each animal was confined to the start and subsequent two alleys for 4 min, and for 6 min in the last (goal) alley, where three food pellets were present in the food cup. This acclimation period promotes stable and high levels of activity on the subsequent training day. On the training day, each animal was placed in the start box and allowed to traverse the maze until it reached the goal box and consumed the single food pellet present in the cup. Upon consuming the food, the animal was returned to its home cage for a 20 min interval (ITI), during which the apparatus was cleaned. After the ITI, the mouse was returned to the start box to begin the next trial, and the sequence was repeated for five trials. The errors (i.e., a turn in an incorrect direction, including those which result in path retracing) made before entering the goal box were recorded on each trial.
126.96.36.199.2. One-Trial Passive Avoidance
A chamber illuminated by dim (<20 lux) red light was used for training and testing. Animals were confined to a circular (“safe”) chamber (10 cm diameter, 8 cm high). The walls and floor of this chamber were white, and the ceiling was translucent orange. The floor was comprised of plastic rods (2 mm diameter) arranged to form a pattern of 1 cm square grids. A clear exit door (3 cm square) was flush with the floor of the safe compartment, and the door was able to slide horizontally to open or close the compartment. The bottom of the exit door was located 4 cm above the floor of a second circular chamber (20 cm diameter, 12 cm high). This “unsafe” chamber had a clear ceiling and a floor comprised of 4 mm wide aluminum planks that formed a pattern of 1.5 cm square grids oriented at a 45° angle relative to the grids in the safe compartment. When an animal stepped from the safe compartment through the exit door onto the floor of the unsafe compartment, a compound aversive stimulus comprised of a bright (550 lux) white light and a “siren” (60 dBc above the 50 dB background) was presented.
Animals learn to suppress movement to avoid contact with aversive stimuli. This “passive avoidance” response is exemplified in step-down avoidance procedures, where commonly, an animal is placed on a platform, whereupon stepping off of the platform it encounters a footshock. Following just a single encounter with shock, animals are subsequently reluctant to step off of the safe platform. The animals’ reluctance to leave the platform is believed not
to reflect fear, because typical fear responses are not expressed in animals engaged in the avoidance response [26
]. So as not to duplicate stimuli between tasks (see associative fear conditioning, above), upon stepping off the platform, animals here were exposed to a compound of bright light and a loud oscillating noise rather than shock. Like more common procedures, our variant of this task supports learning after only a single trial (i.e., subsequent, step-down latencies will be markedly increased).
Animals were placed on the platform behind the exit blocked by the Plexiglas door. After 4 min of confinement, the door was retracted and the latency of the animal to leave the platform and make contact with the grid floor was recorded. Prior to training, step-down latencies typically range from 8–20 sec. Upon contact with the floor, the door to the platform was closed and the aversive stimulus (light, noise, and vibration) was presented for 4 sec, at which time the platform door was opened to allow animals to return to the platform, where they were again confined for 5 min. This ITI is sufficiently long to demonstrate learning as opposed to recovery from the aversive stimuli [6
]. At the end of this interval, the door was opened and the latency of the animal to exit the platform and step onto the grid floor (with no aversive stimulation) was recorded. The ratio of post-training to pre-training step-down latencies was calculated for each animal and served to index learning. It has been determined that asymptotic performance is apparent in group averages following 2–3 training trials; thus performance after a single trial reflects, in most instances, sub-asymptotic learning.
188.8.131.52.3. Associative Fear Conditioning
Two distinct experimental chambers (i.e., contexts; 32 l × 28 w × 28 cm h) were used, each of which was contained in a sound-and light-attenuating enclosure. These boxes were designated as “training” and “testing” contexts, and differed as follows: The training context was brightly illuminated (100 lux), had clear Plexiglas walls, no lick tube, and parallel stainless-steel rods (5 mm, 10 mm spacing) forming the floor. The test context was dimly illuminated (6 lux) the walls were covered with an opaque pattern of alternating black and white vertical stripes (3 cm wide), and the floor was formed from stainless-steel rods arranged at right-angles to form a grid of 8 mm squares. A water-filled lick tube protruded through a small hole in one wall of the test chamber, such that the tube’s tip was flush with the interior surface of the wall at a point 2 cm above the floor. Upon contacting the tube, the animal completed a circuit such that the number of licks per second could be recorded. This circuit was designed so that if an animal makes continuous contact with the tube (i.e., “mouthed” the tip), the circuit recorded 8 licks per second, a rate that approximates constant licking.
In this procedure, animals were exposed to a stimulus (i.e., a CS; white noise) that terminated at the onset of a mild footshock (i.e., a US). These white noise-shock (CS-US) pairings come to elicit conditioned fear responses when animals are subsequently presented with the white noise. This learned fear can be assessed in various ways. In the present studies, fear was indexed by CS-elicited suppression of ongoing drinking, as this measure is easily and precisely quantified. “Lick suppression” is conceptually analogous to the more commonly used measure of CS-elicited generalized “freezing” (i.e., during that time in which an animal freezes it will necessarily suppress its approach to and drinking from a lick tube). In our laboratory, lick suppression has proven to be of greater utility, given that the generalized freezing exhibited by mice is far less regular, and thus more ambiguous, than that typically observed in rats. To avoid any interaction with the training context, which itself acquires an association with shock (and the capacity to evoke fear), with the CS at the time of testing, training and testing were conducted in separate distinct contexts.
In the training chamber, a 0.6 mA constant-current scrambled footshock (US) was delivered through the grid floor. In both the training and test chambers, a 40 dB above background white noise CS was presented through speakers mounted at the center of the chamber’s ceiling.
Water bottles were removed from the animals’ cages near the offset of the light cycle on the day prior to acclimation. Water-deprived animals were then acclimated to the training and test chambers by placing them each in both contexts for 10 min on the day prior to training. Within several minutes of their first placement in the test context, water-deprived mice exhibit stable licking. When subsequently placed in the chamber, these animals will initiate licking within 5–10 sec and lick at relatively stable rates for the subsequent 3–5 min. Animals were given their water bottles for 90 minutes prior to the offset of the light cycle at the end of the acclimation day and the training day. Training occurred in the training context in a single 20 min session during which each animal was administered a white noise-shock pairing 7 and 14 minutes after entering the chamber. Each 10 sec white noise terminated with the onset of a 500 msec footshock. Asymptotic performance (as evidenced in group means) has been observed with these parameters after 4–6 such pairings. Thus, two pairings, in most instances, supports sub-asymptotic conditioned responding. At the end of the training session, animals were returned to their home cages for 60 min, after which they were re-acclimated to the test context for 10 min where they were allowed free access to the lick tubes. On the subsequent day (23–25 hours post-training), animals were tested. Each animal was placed in the test context whereupon after making 25 licks, the noise CS was presented continuously until the animal completed an additional 25 licks. The latency to complete the 25 licks during the pre-tone interval and in the presence of the one was recorded, with a 600 sec limit imposed on the second 25 licks, a limit not reached by any animal described here. With these measures, the ratio of latency to complete 25 licks in the presence of the CS to the latency to complete 25 licks prior to CS onset served as our index of learned fear.
184.108.40.206.4. Odor Discrimination and Choice
A black Plexiglas 60 cm square field with 30 cm high walls was located in a dimly lit (20 lux) testing room with a high ventilation rate (3 min volume exchange). Three 4L × 4W × 2 cm H aluminum food cups were placed in three corners of the field. A food reinforcer (30 mg portions of chocolate flavored puffed rice) was placed in a 1.6 cm deep, 1 cm diameter depression in the center of each cup. The food in two of the cups was covered (1.0 cm below the surface of the cup) with a wire mesh so that it was not accessible to the animal, while in the third cup (the “target” cup), the food was able to be retrieved and consumed. A cotton-tipped laboratory swab, located between the center and rear corner of each cup, extended vertically 3 cm from the cups’ surface.
Rodents rapidly learn to use odors to guide appetitively-reinforced behaviors. In a procedure based on one designed by Sara [28
] for rats, mice learned to navigate a square field in which unique odor-marked (e.g., almond, lemon, mint) food cups were located in three corners. Although food was present in each cup, it was accessible to the animals in only one cup, the one marked by mint odor. An animal was placed in the empty corner of the field, after which it explored the field and eventually retrieved the single piece of available food. On subsequent trials, the location of the food cups was changed, but the accessible food was consistently marked by the same odor, mint. On successive trials, animals required less time to retrieve the food and made fewer approaches (i.e., “errors”) to those food cups in which food was unavailable. Using this procedure, errorless performance is typically observed within 3–4 training trials.
Immediately prior to each trial, fresh swabs were loaded with 25 ul of either lemon, almond, or mint odorants (McCormick flavor extracts). The mint odor was always associated with the target food cup. It should be noted that in pilot studies, the odor associated with food was counterbalanced across animals, and no discernible differences in performance could be detected in response to the different odors.
Food deprivation occurred in the same manner as it did in Lashley Maze. The night that food was removed from the animals’ cages, two chocolate flake reinforcers were placed in the home cage. The next day would normally be an acclimation day, but instead animals were given 60 minutes of free feeding at the same time of day they would have received it had they been acclimated to the apparatus. On the subsequent test day, animals received four training trials in the field with the three food cups present. On each trial, an animal was placed in the empty corner of the field. On Trial 1, the reinforcing food was available to the animal in the cup marked by mint odor. An additional portion of food was placed on the top surface of the same cup for the first trial only. The trial continued until the animal retrieved and consumed the food from the target cup, after which the animal was left in the chamber for an additional 20 sec and then returned to its home cage to begin a 6 min ITI. On Trials 2 through 4, the location of the food cups was re-arranged, but the baited cup remained consistently marked by the mint odor. On each trial, the latency to retrieve the food and errors were recorded. An error was recorded any time an animal made contact with an incorrect cup, or its nose crossed a plane parallel to the perimeter of an incorrect cup. Similarly, an error was recorded when an animal sampled (as above) the target cup but did not retrieve the available food.
220.127.116.11.5. Spatial Water Maze
A round black pool (140 cm diameter, 56 cm deep) was filled to within 24 cm of the top with water made opaque by the addition of a nontoxic, water soluble, black paint. A hidden 11 cm diameter perforated black platform was in a fixed location 1.5 cm below the surface of the water midway between the center and perimeter of the pool. The pool was enclosed in a ceiling-high black curtain on which five different shapes (landmark cues) were variously positioned at heights (relative to water surface) ranging from 24–150 cm. Four of these shapes were constructed of strings of white LED’s (spaced at 2.5 cm intervals) and included an “X”(66 cm arms crossing at angles of 40° from the pool surface), a vertical “spiral” (80 cm long, 7 cm diameter, 11 cm revolutions), a vertical line (31 cm) and a horizontal line (31 cm). The fifth cue was constructed of two adjacent 7W light bulbs (each 4 cm diameter). These cues provided the only illumination of the maze, totaling 172 lux at the water surface. A video camera was mounted 180 cm above the center of the water surface.
For this task, animals were immersed in a round pool of opaque water from which they can escape onto a hidden (i.e., submerged) platform. The latency for animals to find the platform decreased across successive trials. In this task, performance of animals can improve across trials despite the animals beginning each trial from a new start location. As demonstrated by Morris [29
], rats performance in the water maze does not rely on fixed motor patterns (i.e., performance improves despite the animal’s irregular starting location) or the presence of discernable cues within the maze (e.g., visual, tactile, or olfactory signals). Instead, performance is dependent on the stability of extra-maze cues, or “landmarks”, and is said to reflect the animals’ representation of its environment as a “cognitive map.”
We have developed a protocol in which mice exhibit significant reductions in their latency to locate the escape platform within ten training trials. In our protocol, animals were confined in a clear Plexiglas cylinder on the safe platform for 5 min on the day prior to training. Second, a 10-minute inter-trial interval (ITI) was used, which is considerably longer than is typical (c.f., 90 sec). Lastly, the maze, surround, and water were black with visual cues that were constructed of patterns of lights.
On the day prior to training, each animal was confined to the escape platform for 300 sec. Training was conducted on the two subsequent days. On Day 1 of training, animals were started from one of the three unique locations on each of six trials. The pool was conceptually divided into four quadrants, and one starting point was located in each of the three quadrants that did not contain the escape platform. The starting point on each trial alternated between the three available quadrants. An animal was judged to have escaped from the water (i.e., located the platform) at the moment at which four paws were situated on the platform, provided that the animal remained on the platform for at least 5 sec. Each animal remained on the platform for a total of 20 sec, after which the trial was terminated. Trials were spaced at 10 min intervals, during which time the animals were held in their home cages. On each trial, a 90 sec limit on swimming was imposed, at which time any animal that had not located the escape platform was placed by the experimenter on to the platform, where it remained for 20 sec. Animals were observed from a remote (outside of the pool’s enclosure) video monitor, and animals’ performance was recorded on video tape for subsequent analysis. Day 2 of training proceeded the same as Day 1, albeit with four trials only. 60 minutes after the 10th trial the hidden platform was removed from the pool and animals were placed inside the maze for a 90 second probe trial.
18.104.22.168. Object Exploration & Habituation
In this task, animals were exposed to two objects (distinct Fisher Price, Little People animal and human figures) placed directly underneath two holes (spaced 2 cm under the opening) in a hole board consisting of an arena (35×52×18 cm rectangle with a black Plexiglas bottom and walls) positioned in front of a shield of white Plexiglas and illuminated by a dim (10 W) light placed behind the shield, so as to minimize the light. This task consisted of two conditions, differential habituation and asymptotic habituation, both of which occurred in this hole board apparatus. The order of the conditions was counter-balanced. Prior to each condition, animals were acclimated to the apparatus for 20 minutes on each of three consecutive days.
In the differential habituation condition, all animals were allowed to explore the same two objects for three trials of 300s followed by a 90s inter-trial interval (ITI), during which the animal was returned to its home cage and the apparatus and object were cleaned with a 67% alcohol solution. One day later, animals were returned to the apparatus for three more trials. On the first trial, the animal was allowed to explore the same two objects it experienced on the previous day. This was intended to mitigate any degradation of long-term memory as well as any initial burst of activity or dishabituation that could be present on the first trial. Prior work had determined that this amount of exposure supported sub-asymptotic levels of habituation to the two target objects. On the second and third trials, one of the two objects was replaced with a novel object, counter-balanced for which object was replaced. Of interest in this condition is the ratio of exploration of the novel object to exploration of the familiar object.
In the asymptotic habituation condition, all animals were exposed to the same objects for an extended period of time until each reached a set habituation criterion. Because animals habituate at different rates, this time period was different for all animals. Here, habituation was quantified after each trial until the animal reached a criterion of five successive trials over the course of two days in which the animal s mean time spent on object exploration (summed between both objects) is 15 seconds or less and equal to 28% or less of their total time spent on object exploration in their most active trial on the first day. Mice reached this criterion across a range of 4 to 11 days (notably, a minimum of one day more than was allotted in the differential [preasymptotic] habituation condition described above). On the following day, animals were exposed to a novel object in the same manner as in the differential habituation condition. Of interest in this condition is the number of trials taken to reach the asymptote criterion in addition to the measure taken to assess novel object exploration in the differential habituation condition.
22.214.171.124. Open Field
Assessment in the open field was performed as in Experiment 1, although here, behavior was monitored for 12 instead of 4 min. For data analysis, the 12 min was divided into three 4-min bins and time spent in open and walled quadrants for each of these time bins were recorded for each animal. Exploration during the first 4-min bin constituted the measure of open field exploration previously found to correlate with learning abilities. Measuring exploration in the second and third time bins enables comparison of the relationship between learning abilities and exploration in both early and later time points in the animals bout of exploration (where different levels of the habituation to the periphery of the field would presumably have been attained). Analysis involved converting animals individual percentages of crossings made in the interior of the field to z-scores relative to their experimental cohorts. To correlate open field performance with general learning abilities, factor scores (representative of aggregate learning performance) were also obtained relative to the animals experimental cohorts.
Consistent with previous findings, positive correlations were found between animals performance on all learning tasks (). These data were subjected to a principal component factor analysis. A single factor accounted for approximately 40% of the variance in the performance of individuals across all learning tasks (). Although the sample size here is small, this degree of explanatory variance is comparable to that observed in prior studies [6
] with larger sample sizes and different combinations of learning tasks. Factor scores were extracted from this analysis to serve as an index of animals aggregate performance across all tasks (i.e., their general learning abilities). (A factor score is closely analogous to an average z score of an animal s performance on each learning task, where the scores are weighted according to the loading of each individual task on the primary factor.)
Correlations (n=24) of Learning Tasks and Exploration in the open field.
Principal Components Analysis (n=24). Variables reflect performance of animals on five learning tasks as well as exploration in an open field.
Consistent with results of previous analyses, the percentage of entries into open quadrants of a walled open field during an initial 4-min period was significantly correlated with individuals aggregate performance (i.e., factor scores) on all learning tasks, r(43) = −.31, p < .05 (). Note here that the negative correlation indicates that animals which performed more efficiently on the learning battery made a larger percentage of their open field crossings in the unwalled portions of the field, i.e., they engaged in more exploration. Furthermore, performance in this first 4 min loaded at .40 with animals performance on the learning tasks on the same principal factor (). However, across the full 12-minute session in the open field, this relationship diminished numerically and fell below the threshold of statistical significance in the subsequent two 4-min time bins, r(43) = −.14, n.s. and r(43) = .03, n.s. respectively ().
Exploration in an open field predicts general learning performance during intial, but not late, exposure to the novel field
In the object exploration task, two measures of novel object exploration were taken. One of these measures was taken after an equal (subasymptotic) number of exposure trials for every animal, and therefore, the degree of habituation to the two sample objects can be assumed to vary across subjects at the time that the novel object was introduced. In this condition, a correlation was found between novel object exploration and general learning ability, r(22) = −.47, p < .02 (). Another measure of exploration of a newly-introduced object was taken after individual animals reached an equal habituation criterion to the familiar sample objects, requiring a different number of exposures (for each animal) to the two sample objects prior to the introduction of the novel object. In this manner, habituation levels to the familiar object was equated across all animals at the time at which the novel object was introduced. In contrast to the condition where habituation levels varied across animals, no correlation between novel object exploration and general learning abilities was observed when animals were equally habituated to the companion (familiar) object, r(22) = −.01, n.s., ().
Exploration of a novel object is correlated with general learning ability when the level of habituation to a comparison object varied across individual animals
The dependence of the relationship between general learning abilities and exploration upon rates of habituation is further supported by the analysis of the top and bottom quartile of learners. In the first 4-min time bin of the open field test, the highest quartile of learners (n = 13) displayed significantly greater exploration of open quadrants than the lowest quartile (n = 13), t(24) = 2.87, p < .05 (). However, when exploration was measured in the last 4-min time bin, when habituation had presumably impacted the performance of both subsets of animals, both groups explored the open quadrants to a similar degree, t(24) = 0.42, n.s.
Animals of higher general learning performance are more exploratory early, but not late, when exposed to a novel field or object
A similar pattern of results were observed for novel object exploration in the hole board task. In the differential habituation condition (where the level of habituation varied across animals), the top quartile of learners (n = 5) exhibited significantly greater exploration of a novel object than the lowest quartile of learners (n = 5), t(8) = 2.80, p < .05 (). In contrast, in the asymptotic habituation condition (where the level of habituation was equated across animals), both groups of learners explored the novel object to a similar degree, t(8) = .78, n.s. Further, the level of exploration of the novel object was similar to that of the top quartile of learners in the differential habituation condition. In both cases, when habituation rates had a minimal influence on exploration, the lower quartile of learners explored no less than the top quartile of learners, indicating that faster rates of habituation drive better learners to explore more at an earlier time point.
Based on the outcomes of prior experiments [23
], here we proposed the possibility that differential rates of habituation (between animals of high and low general learning abilities) might mediate the relationship between general learning abilities and tests of exploration (such as in a novel open field). To assess this possibility, we proposed that levels of habituation could be manipulated such that they are either variable or held constant across a sample of mice, and suggested that only measures of exploration taken when habituation levels are variable across animals should correlate with those animals general learning abilities. In contrast, measures of exploration obtained when habituation levels are comparable across animals should be unrelated to general learning performance.
In two independent tasks, the present experiment provides evidence consistent with the above hypotheses. Early during a period of exposure to an open field (where levels of habituation are presumably most variable across mice), a relationship between general learning abilities and measures of exploration were correlated such that animals of higher general learning abilities exhibited more exploration (i.e., more time in the center, unwalled portions of the field). However, at later time points, where habituation to the walled portions of the field would have been more complete (and comparable across animals), the relationship between general learning abilities and exploration was no longer observed. In a nose poke exploration task, when levels of habituation to two sample objects were free to vary (owing to an equal but sub-asymptotic number of exposure sessions), a relationship existed between general learning abilities and measures of exploration of a novel object (that replaced one of the familiar objects). However, when levels of habituation to the familiar objects were equated across mice (by terminating exposure for each individual when a common habituation criterion was reached), the level of exploration of a new object did not differ across animals of high and low general learning abilities. Thus in both of these tasks, the relationship between general learning ability and exploration was only observed when habituation levels (either to a novel environment or object) varied across animals at the time of critical testing. This pattern of results provides strong evidence that habituation (itself a form of learning) mediates the relationship between general learning abilities and exploratory behaviors.
It is important to note that in the open field, the relationship between general learning abilities and exploration did not diminish over time due to a reduction
in exploratory behaviors in animals with the highest general learning performance. Rather, after prolonged exposure to the open field, animals of higher general learning ability continued to express high levels of exploration, while animals of lower general learning ability increased exploratory behaviors to a level comparable to that of their faster learning counterparts. It should also be noted here that a similar pattern has been observed when animals received extensive training on other learning tasks. That is, animals learning
performance on early trials (i.e., during acquisition) was more highly correlated with general learning abilities than was their performance on later (asymptotic) trials [7
]. Based on both the present data and these earlier observations, it thus appears that patterns of “exploration” are, at least in part, a reflection of the rate at which animals learn about a novel environments (or objects), and rather than reflecting only
a native behavioral tendency, is an expression (in part) of an animal s general learning ability.