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Effects of Rearing Environment and Sex on Maze Learning, Memory, and Competitive Exploration.
by Rhawn Joseph,
Veterans Affairs Medical Center, Departments of Pharmacology and Psychology, Nashville, Tennessee
Reprinted from: Journal of Psychology, 101, 37-43, 1979.

ABSTRACT

Male and female rats reared in enriched or deprived environments were tested for maze learning ability, retested for retention after 30 days (Experiment 1, N= 22), and tested for exploratory behavior, defined as the competing tendency to make irrelevant ìsection entryî responses when allowed unobstructed, problem-free access to goal boxes (Experiment 2, N=16). It was found that enriched and deprived males (a) demonstrated a superior maze learning ability as compared to enriched and deprived females, respectively; (b) enriched rats were superior maze learners and more exploratory than deprived rats and demonstrated superior long-term memory; and (c) enriched males were more exploratory than enriched females, whereas deprived females were more exploratory than deprived males. It was concluded that differential rearing conditions may cause significant reversals in sex related ability and behavior (i.e., maze learning and exploration) and may significantly affect perceptual sensitivity as well as significantly impact learning ability and long-term memory.

INTRODUCTION

Several studies have shown that rats reared in enriched environments during the early postweaning periods make fewer errors on the Hebb-Williams maze than those reared in standard laboratory cages (1, 5, 9). Other reports, however, have suggested that the maze learning superiority of rats reared with enriched experiences may be due to a reduction of exploratory drive (9, 10). This position is based on the findings that enriched rats are less active than deprived rats.

In apparent contradiction to these reports, Brown (1) and Denenberg and Morton (3) found no differences between enriched and deprived ratsí open field ìexploratoryî activity, whereas Gardner et al. (4) discovered that perceptually enriched animals were significantly more exploratory than deprived ones. In addition, a recent report (8) has indicated that though deprived rats are indeed more active (exploratory) than enriched ones, there is no relationship between open field ambulation scores and maze learning performance.

A major source of confusion in the attempt to define the role of exploration in maze learning is the assumption that exploratory behavior is similarly aroused in an open filed containing little or no complexity, and in a complex maze learning task in which the Ss have been food deprived for 18 to 23 hours. It seems that error accruing responses on a maze problem can only be attributed to exploratory behavior in hungry animals, when the competing stimuli relevant to hunger, as well as the novel distractions of a complex environment, are maintained for comparative purposes across all measures of behavior.

The purpose of the present study was to determine the effects of proprioceptive and visual enrichment or impoverishment during the early life of rats on their learning ability, memory, and exploratory behavior. Exploration was defined and measured as a competing tendency to make irrelevant error-accruing responses on a maze field that was problem free. As in maze problems, goal directed behavior was maintained and rewarded in the measures of exploration.

In addition, the present study examined the factor of information storage or memory in the maze learning process. Hence, all Ss were trained to criterion on the first set of maze problems, then retested so as to provide a possible index of differential memory capacity.

B. EXPERIMENT 1

1. Method

a. Subjects. Holtzman rats (12 males and 10 females) born from four mothers were weaned and began the experiment at approximately 20 days of age. Pups were assigned by the split littler technique to one of four conditions: enriched males (N=6), enriched females (N=5), restricted males (N=6), restricted females (N=5). All Ss were maintained on Purina lab chow and water ad lib, except when training and testing procedures called for hunger motivation.

b. Rearing cages. One large rearing cage (1.218 x .4568 x .3045 m) divided into separate halves to segregate the sexes was used for the enriched environmental rearing condition. Restricted Ss were housed individually in standard laboratory cages (25.4 x 12.7 x 17.78 cm).

c. Isolation chamber. Restricted Ss were housed in their cages in a large sound-proofed isolation chamber (1.827 x .9135 x .609 m) for the first 80 days of life postweaning. The chamber had six shelves with two cages per self. Cages were further insulated from sound by a double layer of .317 cm cardboard which surrounded all four walls of each cage with a small opening in front for light. Each shelf served as both floor for the cage above and roof for the cage below. The door of the chamber contained a small window (.609 x 4507 m) which allowed light to enter.

d. Rearing conditions. Following environmental assignment, restricted Ss were not handled again until they reached approximately 100 days of age. Those in the enriched condition were handled frequently, several times each day for the first 45 days of life postweaning.

During the first 45 days of enriched environmental conditioning the home cage was shifted about the colony room every other day. The cage was also enriched by a daily change of objects (i.e., blocks, bottles, corks, mouse cages, cups, ladders) which were periodically removed, replaced, or introduced briefly. Every other day males were removed and placed in the female half of the cage and vice versa. After the initial 45 days, these procedures were changed to once a week.

At approximately 100 days of age all Ss were removed from their respective environmental conditions and housed individually in standard rack ages. In addition, all Ss were briefly handled daily for 20 days prior to testing so as to minimize cage emergence stress.

At approximately 120 days of age all Ss were weighed and immediately placed on a 23 h food deprivation schedule for the remainder of Experiment 1. When all Ss had lost 15-20% of their free-feeding weight they begin training and then testing according to the procedures outlined by Joseph et al. (7). Unfortunately, prior to the onset of training, two restricted males, one restricted female, and one enriched female had died, and during the course of training, but prior to onset of testing, one enriched male and one additional female died.

e. Procedure. All Ss were trained and tested in a symmetrical maze (2) described in detail by Joseph et al. (7). Ssí performances were monitored via a video TV camera positioned directly 8 feet above the maze. Extraneous sound was masked with 25 db white noise, and all observations were made in a room separate from the maze.

Seven maze problems (2) were used as measures of learning ability (T-3, T-7 through T-12). Procedures outlined by Joseph et al. (7) were utilized for scoring trials and errors. Ss were tested every other day.

Upon completion of the last test all Ss were returned to ad lib feeding for 30 days, at the end of which they were again placed on the food deprivation schedule, reduced to 80-85% of their weight, and then retested with the same procedure and maze sequence, with the exception that all Ss were run daily.

2. Results

A 2 x 2 x 2 factor analysis of variance was performed for sex, rearing condition, and learning vs. relearning, with total trials and errors taken to learn the maze problems as the dependent measures. There was a significant main effect for sex with males taking fewer trials, p < .05, and making fewer errors, p< .005, than females. A significant main effect for rearing condition was found, supporting previous findings that enriched Ss make fewer errors, p< .005, and require fewer trials, p < .01, in learning maze problems than restricted Ss. A main effect for relearning was discovered for trials, p < .005, and errors, p< .001. There was also a significant interaction between sex and relearning, such that females made a greater improvement in their second maze learning performance (errors to completion) than males, p< .05.

3. Discussion

Evidence presented in this paper demonstrates that when rearing conditions were similar, maze learning was an ability at which males excelled. This conclusion is supported by other reports which show females did not learn maze problems as quickly as males (2, 6, 7). However, the finding that females made greater improvements in relearning than males suggests that these differences can be diminished with practice. However, males continued to outperformed females significantly during the second maze series. Nevertheless, though maze learning appeared to be a male linked ability, restricted males did not perform as well as did the enriched females. Thus it would appear that rearing condition is a powerful variable which can counteract established learning differences related to sex (6).

The finding that all Ss significantly improved their second maze series performance suggests no differences in the memory mechanisms which contributed to the learning process. However, the finding that the sex and environmental differences were maintained during the second test, even though all Ss had learned the first maze series, suggest that this result may be misleading and that long term memory is significantly effected among animals reared in a deprived or impoverished environment.

C. EXPERIMENT 2

1. Method

The same Ss used in Experiment 1 participated in Experiment 2. Upon completion of the second series of maze problems, all Ss were given food and water ad lib for three days. On the fourth day all Ss were again placed on a 23 hour per day food deprivation schedule, reduced to 80-85% of their ad lib weight, and on the seventh day they were tested for competitive behavior.

In each measure, a clear path was maintained between the two goal boxes of the Davenport maze (2), providing all Ss with an unobstructed problem-free path. On either side of the open path, barrier boards were set up symmetrically, as in the maze problems, creating alleys and tunnels which could be freely explored. As in the maze problems, goal seeking heavier was maintained, and all Ss were rewarded with two Noyes food pellets for shuttling between goals boxes.

Ss were run for four consecutive days on four slightly different open/maze fields. Two of the exploratory measures were structurally different in terms of barrier board placements (E-1 and E-3), and two of the measures (E-2 and E-4) were structurally similar to measures E-1 AND E-3, respectively, except that small 2.54 cm square black blocks were attached to the wire mesh floor, 3.81 cm inside each section (exploratory zone), thereby creating two ìadded noveltyî conditions. Hence, there were a total of four exploratory measures, two of which measured responses to added novelty. The four were run sequentially over a four day period, one per day.

Each S was allowed to run one exploratory field per day for a total of 12 trials per measure. Entering alley or maze tunnel (exploratory zone) or making contact with the wooden block inside the error zone was scored as a ìsection entry.î In addition, fecal pellets and time spent between goals in the open/maze exploratory field were recorded. The procedures utilized for testing maze learning (7) remained the same for these measures.

2. Results

A 2 x 2 x 2 x 2 factor analysis of variance was performed on the data comparing sex, rearing condition, added novelty, and sequence of barrier design. No significant main effects were found for sex. There was a significant main effect for environment such that enriched Ss made more section entries than restricted Ss, p< .004. A significant interaction was found between sex and rearing however, p< .005, such that enriched males were more exploratory than enriched females, whereas restricted females were more exploratory than restricted males. Enriched Ss were found to be significantly more responsive to the added novelty conditions, making more exploratory errors than restricted Ss, p< .05. A main effect was also discovered for sequence of and exploratory barrier design, p< .001, such that enriched Ss were more exploratory on measures E-1 and E-2 than E-3 and E-4, p< .01. No other significant differences were found.

3. Discussion

Animals reared in an enriched vs deprived environment, display suprior learning ability, superior retention and long term memory, and a greater degree of curiosity and exploratory behavior.

The finding that enriched Ss explored more than those reared in a restricted environment is in contradiction to previously presented evidence (1, 3, 8, 9, 10), but is supported by recent findings (6). This is most likely a result of differences in motivation: in these previous studies, hunger motivation was not present in the exploratory tasks as it was during the measure of behavior in the present study and another similar one (6).

Furthermore, in comparison to the paradigm employed in the present study, the open field measure of "exploration" offered little novel or complex stimulation, nor was goal directed behavior maintained as was done in the present experiment. Hence differences in results are hardly comparable. Nevertheless, in light of the data presented herein, it seems that open field measures of activity should not be generalized across testing conditions and used as an explanation for the poor maze learning performance of restricted rats.

A striking feature of the restricted Ss used in the present study was their relatively low level of exploratory behavior and significant deficits in learning and long-term memory. These findings indicate either a lack of exploratory drive or a failure to differentiate visual cues in the environment (1, 5), which might have induced exploratory behavior. The high level of exploration in enriched males suggests, when coupled with their superior maze learning performances, that attentiveness to novel cues may have aided in their learning the correct maze path. Conversely, that females demonstrated poor maze learning ability (2, 6, 7) yet maintained high levels of exploration, suggest that their poor performance may have been due to distractibility (6, 7). Moreover, it is possible that in restricted Ss the well learned shuttling sequence between goal boxes became a dominant, perseverative pattern of responding which overrode any competing exploratory tendencies (6).


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