Table 1.
Summary of behavioral changes in experimental models of TBI
Table 1. Overview of the current literature organized by type of memory disrupted after experimental TBI. Abbreviations: d, day; CCI, controlled cortical impact; FPI, fluid percussion injury; ITI, inter-trial time; mod, moderate; LFPI, lateral fluid percussion injury; MWM, Morris water maze; PID, post injury days; rec, recent; ref, reference; rem, remote; sec, seconds; TOR, temporal order recognition memory.
| Ref | Injury Model | Animal age and gender | Animal group | Memory Task Protocol | Test performance PID | Behavioral effects (TBI vs Sham) | p value |
|---|---|---|---|---|---|---|---|
| Working memory | |||||||
| Kobori et al (2006) | Moderate-severe CCI | Adult male rats | Sham: 8 TBI: 8 |
MWM working mem Training: 5 trials with 5 sec delay between sample and choice phase and 4 min ITI Test: the following day |
13–14 and 27–28 | ⇑ latency to reach the platform at 14 and 28 PID | p<0.001 |
| Hoskinson et al (2009) | Moderate-severe CCI | Adult male rats | Sham: 6 TB:I 10 |
MWM working mem Training 5 trials with 5 sec delay between sample and choice phase and 4 min ITI for 1 day followed by test Swim T maze: 10 training trials/d for 7 d (10 s ITI) followed by 5 d testing |
120 (3 months) | ⇑ latency to reach the platform in MWM task | p<0.05 |
| ⇓ correct choice percentage with the same amount of training in swim T maze | p<0.001 | ||||||
| Sebastian et al (2013) | CCI | Adult male rats | Sham: 3–4 TBI: 3–4 |
Radial 8-arm maze Training: 10 trials/d for 6 d starting at 21 PID Test: 3–5 trials followed by test at 42 PID |
42 (5 weeks) | ⇑ number of working memory errs | p<0.05 |
| Both groups (Sham & TBI) improved performance over days | p<0.001 | ||||||
| Sebastian et al (2013) | CCI | Adult male rats | Sham: 3–6 TBI: 3–6 |
Radial 8-arm maze Training: 10 trials/d for 6 d starting at 42 PID Test: 3–5 trials followed by test at 63 PID |
63 (9 weeks) | ⇑ number of working memory errs during training | p<0.001 |
| No difference during test | NS | ||||||
| Lyeth et al (1990) | Mild – Moderate LFPI | Adult male rats | Sham: 8 TBI mild: 7 TBI mod: 10 |
Radial 8-arm maze Training: 1 session per day (10 sec ITI) until < 1 err/d for 3 consecutives days before TBI |
5 – 25 | Impaired working memory performance up to 5 PID in mild TBI | p<0.05 |
| ⇑number of working memory err up to 15 PID in moderate TBI | p<0.05 | ||||||
| Intact ref memory | NS | ||||||
| Whiting et al (2006) | Moderate LFPI | Adult male rats | Sham: 9 TBI: 10 |
Swim T maze Training: 15 trials/d with 7 sec delay between sample and choice phase (11–15 PID). Test: 15, 30, 120 sec between sample and choice phase |
16–18 | No difference with 15 sec delay | NS |
| Impaired working memory performance with delay 30 and 120 sec | p<0.05 | ||||||
| Eakin et al (2012) | Mild LFPI | Adult male rats | Sham: 3 TBI: 3 |
Swim T maze Training: 0 delay between sample and choice phase. Test: 15, 30, 60, 120 delay between sample and choice phase |
30–60 | Impaired working memory performance with delays | p<0.01 |
| Sweet et al (2014) | Moderate midline FPI | Adult male rats | Sham: 6 TBI: 6 |
Swim T maze Training: 0 delay between sample and choice phase for 5 d. Test: 15 trials/d with 60 sec delay between sample and choice phase for 12 d |
3 weeks after electrodes implantation | Impaired working memory performance during test | p<0.01 |
| Smith et al (2015) | Mild/moderate LFPI | Young adult mice | Sham: 9 TBI: 7 |
T maze Training: 10 trials/d with 0 delay per 7 d before TBI Test: immediately after TBI for 7 continuous days |
7 | Impaired working memory performance | p<0.01 |
| Spatial anterograde memory | |||||||
| Hamm et al (1992) | Moderate CCI | Adult male rats | Sham: 8 TBI: 8 |
MWM ref 4 trials/d for 5 d (4 min ITI) |
11–15 & 30–34 | ⇑ latency to reach the platform at both time points | p<0.05 |
| ⇑ time spent in the peripheral part | p<0.05 | ||||||
| Dash et al (1995) | CCI | Adult male rats | Sham: 10 TBI: 10 |
MWM ref 4 trials/d for 5 d (4 min ITI) |
14 | ⇑ latency to reach the platform | p<0.01 |
| Fox et al (1998) | CCI | Adult male mice | Sham: 11 TBI: 15 |
Barnes maze 1 session/d for 4 d |
7–10 | ⇑ escape latency | p<0.05 |
| ⇓ spatial pattern strategy | p<0.05 | ||||||
| Pierce et al (1993) | Moderate LFPI | Adult male rats | Sham: 15 TBI: 12 |
MWM ref 1992 |
7–8 | ⇑ latency to reach the platform | p<0.01 |
| Whiting et al (2008) | Moderate LFPI | Adult male rats | Sham: 8 TBI: 8 |
MWM ref Training: blocks of 3 trials (30 min between blocks) until criteria reached Test: after 4, 8, 24 h |
11–12 | ⇑ trials to reach the criteria | p<0.01 |
| No difference to reach the platform after 4, 8, 24h delay | NS | ||||||
| Fedor et al (2010) | Moderate LFPI | Adult male rats | Sham: 8 TBI: 12 |
Barnes maze Training: 2 trials (2 min ITI) for 3 d |
90 | No difference in the escape latency | NS |
| ⇑ peripheral search strategy | p<0.01 | ||||||
| Hylin et al (2013) | Mild LFPI (1 atm) & Mild LFPI (1.5atm) | Adult male rats | Sham: 17 TBI (1atm): 20 TBI(1.5 atm): 11 |
MWM ref Training: 10 trials/d (4min ITI) for 1 d followed by a probe trial after 30 min |
5 | No difference in the mild (1 atm) group | NS |
| ⇑escape latency during training and probe trial in the mild (1.5 atm) group | p<0.01 | ||||||
| ⇑ peripheral search strategy | p=0.05 | ||||||
| Lee at al (2013) | Moderate LFPI | Adult male rats | Sham: 14 TBI: 13 |
Barnes maze Training: 2 trials (2 min ITI) for 3 d |
5–7 | ⇑escape latency | p<0.05 |
| ⇑ peripheral search strategy | p<0.05 | ||||||
| Zohar et al (2011) | CHI | Adult male mice | Sham: 10 TBI: 10 |
MWM ref Training: 6 trials/d for 4 d and test the following day |
7, 30, 60, 90 | ⇑escape latency | p<0.05 |
| Spatial retrograde memory | |||||||
| Smith et al (1991) | Moderate and severe LFPI | Adult male rats | Sham: 12 TBI mod: 12 TBI sev: 13 |
MWM ref Training: 10 trials/d for 2 days until 2.5 h before TBI Test: 42 h post-injury |
42 h | Impaired task performance | p<0.01 |
| Okiama et al (1992) | Moderate LFPI | Adult male rats | Sham: 11 TBI: 20 |
MWM ref Training: 10 trials/d for 2 days before TBI Test: 42 h post-injury |
42 h | ⇑escape latency | p<0.01 |
| Hicks et al (1993) | Mild LFPI | Adult male rats | Sham: 10 TBI mild: 7 |
MWM ref Training: 10 trials/d for 2 days until 2.5 h before TBI Test: 42 h post-injury |
42 h | Impaired task performance | p<0.05 |
| Smith et al (1994) | Moderate LFPI | Adult male rats | Sham: 11 TBI: 12 |
MWM ref Training: 10 trials/d for 2 days until 2.5 h before TBI Test: 7 PID |
7 | Impaired task performance | p<0.05 |
| Smith et al (1994) | Moderate LFPI | Adult male rats | Sham: 15 TBI: 11 |
MWM ref Training: 10 trials/d for 2 days until 2.5 h before TBI Test: 14 PID |
14 | Impaired task performance | p<0.05 |
| Whiting et al (2008) | Moderate LFPI | Adult male rats | Sham: 8 TBI rec: 8 TBI rem: 8 |
MWM ref Training: 5 trials/d for 5 d (10 min ITI) before (1 or 13 days) TBI Test: at 14 PID a reminder trial and a second probe trial |
14 | No difference with any delays | NS |
| Sebastian et al (2013) | CCI | Adult male rats | Sham: 4 TBI: 4 |
Radial 8-arm maze Training: 10 trials/d for 6 d before TBI Test: 3–5 trials followed by test at 14 PID |
14 | No impairment in ref memory | NS |
| Impaired working memory performance | p<0.05 | ||||||
| Episodic memory | |||||||
| Gurkoff et al (2013) | Moderate LFPI | Adult male rats | Sham: 12 TBI: 11 |
TOR three times 5 min acquisition separated by 15 min interval followed by test |
14 | Impaired temporal order discrimination | p<0.05 |
| Gurkoff et al (2013) | Moderate LFPI | Adult male rats | Sham: 11 TBI: 12 |
Topological task Habituation for 15 min Test after 5 min delay |
14 | No difference in the ability to discriminate a spatial change in the object | NS |
| Gurkoff et al (2013) | Moderate LFPI | Adult male rats | Sham: 9 TBI: 10 |
Metric tsk Habituation for 15 min Test after 5 min delay |
14 | Impaired ability to discriminate a distance change between objects | p<0.05 |
| Zhang et al (2015) | Mild CHI | Adult male rats | Sham: 8 TBI: 11 |
TOR | 45 and 90 | Impaired temporal order discrimination | p<0.05 |