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Review
. 2014;55(2):310-32.
doi: 10.1093/ilar/ilu013.

Assessing spatial learning and memory in rodents

Charles V Vorhees, Michael T Williams
Review

Assessing spatial learning and memory in rodents

Charles V Vorhees et al. ILAR J. 2014.

Abstract

Maneuvering safely through the environment is central to survival of almost all species. The ability to do this depends on learning and remembering locations. This capacity is encoded in the brain by two systems: one using cues outside the organism (distal cues), allocentric navigation, and one using self-movement, internal cues and nearby proximal cues, egocentric navigation. Allocentric navigation involves the hippocampus, entorhinal cortex, and surrounding structures; in humans this system encodes allocentric, semantic, and episodic memory. This form of memory is assessed in laboratory animals in many ways, but the dominant form of assessment is the Morris water maze (MWM). Egocentric navigation involves the dorsal striatum and connected structures; in humans this system encodes routes and integrated paths and, when overlearned, becomes procedural memory. In this article, several allocentric assessment methods for rodents are reviewed and compared with the MWM. MWM advantages (little training required, no food deprivation, ease of testing, rapid and reliable learning, insensitivity to differences in body weight and appetite, absence of nonperformers, control methods for proximal cue learning, and performance effects) and disadvantages (concern about stress, perhaps not as sensitive for working memory) are discussed. Evidence-based design improvements and testing methods are reviewed for both rats and mice. Experimental factors that apply generally to spatial navigation and to MWM specifically are considered. It is concluded that, on balance, the MWM has more advantages than disadvantages and compares favorably with other allocentric navigation tasks.

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Figures

Figure 1
Figure 1
Radial-arm water maze (RWM). Depiction of the RWM with eight arms radiating from a central hub. One arm is always the start, and hidden platforms are located in each of the remaining seven arms at the start of a new session/day (not depicted). After each hidden platform is found, the rat remains on it for 10 seconds and is then placed in a holding cage while that platform is removed. For trial 2, the animal is placed back in the start arm and allowed to freely choose once again. Unlike the appetitive radial-arm maze, in which the animal has no incentive to return to the last arm visited, in the RWM the animal is reinforced to revisit the arm it just found because it escaped at that location on the previous trial. This creates an initial increase in errors in the water version until the rat learns a win-switch or nonmatching to sample rule to not return to the previously visited arm. In this drawing, there are T-shaped structures attached to the floor so the maze may be used in a different configuration by insertion of a structure that rests against these T-shaped guides that are not relevant to the maze's use as a RWM because the T-guides are far below the water level. Drawing courtesy of AB Plastics, Cincinnati, Ohio; reproduced with permission.
Figure 2
Figure 2
Star maze. The Star maze is run in three phases consisting of the following: Day 0 (pretraining): Run with no intentional distal cues present and a visible platform located in arm 7 with the start position always in arm 1. Day 1 (training): Run with intentional distal cues attached to surrounding curtains and the platform located in arm 7 and submerged. This phase continues for 10 sessions, with four trials per session. Day 2 (probe): The animal is now started in arm 5 with hidden platforms in arms 7 and 1 to determine which arm they chose but reinforcing either equally. Reprinted from Fouquet et al. (2013) and reprinted here with permission of the senior author (Dr. Laure Rondi-Reig).
Figure 3
Figure 3
Cincinnati water maze (CWM). Schematic drawing of the CWM. Channels are 15 cm wide throughout. The maze is constructed of black, high-density polyethylene with chemically welded seams (AB Plastics, Cincinnati, OH). Walls are 51 cm high, and the water is filled to a depth of 22 cm. The maze is water-tight and mounted on leveling legs 25 cm in height. “S” is the start location, and “G” is the goal location. A platform submerged 1 to 2 cm below the water surface is positioned at point G. Errors of commission are defined as when an animal's head and two front legs pass an imaginary line between the main channel into the stem of a T, when its head and front legs cross a line into either arm of a T, or when an animal reenters into the start corridor after having left it. Rats receive two trials per day with a trial limit of 5 minutes. Errors and latency to escape are recorded. Data are analyzed as two-trial (day) blocks. Under white light testing, it typically takes 5 or 6 days for proficient learning. Under infrared light, it takes about 15 days. If a rat fails to find the escape within the time limit, it is placed on the platform for 10 seconds and then given a 5-minute rest before trial 2. If a rat finds the escape in less than 5 minutes, it is given trial 2 after 10 seconds on the platform.
Figure 4
Figure 4
Morris water maze (MWM) performance in mice in different size tanks. C57BL/6J adult male mice were randomly divided into two groups of equal numbers and tested in either a 122-cm or 152-cm diameter tank. The maze conditions were identical for both groups. The smaller diameter was achieved by placing an inner ring within the larger diameter tank constructed of the same polypropylene material as the outer tank. Both groups first received cued training trials first for 6 days. Training consisted of 1 day with the start and platform in fixed positions for six trials and 5 days with random start and platform positions for two trials per day. After this, mice received 5 days of acquisition to find a fixed hidden platform for four trials per day from randomized start positions balanced such that they received one trial from each of four start positions each day. The platform was in the SW quadrant and start positions were arranged such that two were from cardinal positions (N and E) and two were from distal ordinal positions (NW and SE) to eliminate very close start positions (W and S). Average latency to reach the platform is shown (mean ± SEM). Because both groups were untreated, latency, path length, and cumulative distance indices all gave the same results. No group differences occurred on training trials. The effect of the pool was not significant. Group sizes were 12 per group.
Figure 5
Figure 5
Morris water maze (MWM) performance in mice given massed or distributed trials. C57BL/6J adult male mice were randomly divided into two groups of equal numbers and tested in a 122-cm diameter tank with either massed (back-to-back) or distributed trials (spaced 10 minutes apart) during hidden platform acquisition. Both groups first received cued training trials for 6 days. Training consisted of 1 day with the start and platform in fixed positions for six back-to-back trials and 5 days with random start and platform positions for two back-to-back trials per day. After this, mice received 6 days of acquisition to find a fixed hidden platform for four trials per day from randomized start positions balanced such that they received one trial from each of four start positions each day. The platform was in the SW quadrant, and start positions were arranged such that two were from cardinal positions (N and E) and two were from distal ordinal positions (NW and SE) to eliminate very close start positions (W and S). Average path length to reach the platform is shown (mean ± SEM). Because both groups were untreated, latency, path length, and cumulative distance indices all gave the same results. There were no significant differences on training trials. There was a significant main effect of trial spacing during hidden platform acquisition: analysis of variance showed a significant effect of group (F(1,21) = 13.11; p < 0.002). The distributed group performed significantly better than the massed group on each day of testing. Group sizes were 12 per group. *p < 0.05 averaged across days.
Figure 6
Figure 6
Morris water maze (MWM) performance in rats given massed or distributed trials. Sprague-Dawley CD IGS (Charles River strain 001) adult male rats were randomly divided into two groups of equal numbers and tested in a 244-cm diameter tank with either massed (back-to-back) or distributed trials (spaced 10 minutes apart) during hidden platform acquisition, reversal, and shift phases with the platform in the SW, NE, and NW quadrants, respectively, and platform sizes of 10, 7, and 5 cm, respectively. Both groups first received acclimation trials in a 244 × 10 cm straight swimming channel (4 trials given back-to-back) on a single day. After this, rats received 6 days of learning to a fixed hidden platform for four trials per day from randomized start positions, balanced such that they received one trial from each of four start positions each day. The platform was in the SW quadrant, and start positions were arranged such that two were from cardinal positions (N and E) and two were from distal ordinal positions (NW and SE) to eliminate very close start positions (W and S). Average latency to reach the platform is shown (mean ± SEM). Because both groups were untreated, latency, path length, and cumulative distance indices gave the same results. There were no significant differences on straight-channel training trials. There was a marginally significant main effect of trial spacing during hidden platform acquisition: analysis of variance showed a nearly significant effect of group (F(1,14) = 4.33; p < 0.06); there were no significant differences on reversal or shift trials. There were no significant group × day interactions. The trial spacing trend on acquisition suggested that the distributed group learned the task faster than the massed group, except on day 6 when the groups converged. Group sizes were eight per group.
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