Functional inactivation of the rat hippocampus disrupts avoidance of a moving object

. 2011 Mar 29 ; 108 (13) : 5414-8. [epub] 20110314

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid21402943

The hippocampus is well known for its critical involvement in spatial memory and information processing. In this study, we examined the effect of bilateral hippocampal inactivation with tetrodotoxin (TTX) in an "enemy avoidance" task. In this paradigm, a rat foraging on a circular platform (82 cm diameter) is trained to avoid a moving robot in 20-min sessions. Whenever the rat is located within 25 cm of the robot's center, it receives a mild electrical foot shock, which may be repeated until the subject makes an escape response to a safe distance. Seventeen young male Long-Evans rats were implanted with cannulae aimed at the dorsal hippocampus 14 d before the start of the training. After 6 d of training, each rat received a bilateral intrahippocampal infusion of TTX (5 ng in 1 μL) 40 min before the training session on day 7. The inactivation severely impaired avoidance of a moving robot (n = 8). No deficit was observed in a different group of rats (n = 9) that avoided a stable robot that was only displaced once in the middle of the session, showing that the impairment was not due to a deficit in distance estimation, object-reinforcement association, or shock sensitivity. This finding suggests a specific role of the hippocampus in dynamic cognitive processes required for flexible navigation strategies such as continuous updating of information about the position of a moving stimulus.

Zobrazit více v PubMed

O'Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971;34:171–175. PubMed

Wilson MA, McNaughton BL. Dynamics of the hippocampal ensemble code for space. Science. 1993;261:1055–1058. PubMed

O'Keefe J, Nadel L. The Hippocampus as a Cognitive Map. Oxford: Clarendon; 1978.

Morris RG, Garrud P, Rawlins JN, O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 1982;297:681–683. PubMed

Pearce JM, Roberts AD, Good M. Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors. Nature. 1998;396:75–77. PubMed

Sutherland RJ, McDonald RJ, Hill CR, Rudy JW. Damage to the hippocampal formation in rats selectively impairs the ability to learn cue relationships. Behav Neural Biol. 1989;52:331–356. PubMed

Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry. 1957;20:11–21. PubMed PMC

Squier LR, Cohen NJ. Human memory and amnesia. In: Lynch G, McGaugh JL, Weinberger NM, editors. Neurobiology of learning and memory. New York: Gilford; 1984. pp. 3–64.

Squire LR, Alvarez P. Retrograde amnesia and memory consolidation: A neurobiological perspective. Curr Opin Neurobiol. 1995;5:169–177. PubMed

Gaffan D. Recognition impaired and association intact in the memory of monkeys after transection of the fornix. J Comp Physiol Psychol. 1974;86:1100–1109. PubMed

Mishkin M. Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature. 1978;273:297–298. PubMed

Sutherland RJ, et al. Retrograde amnesia after hippocampal damage: Recent vs. remote memories in two tasks. Hippocampus. 2001;11:27–42. PubMed

Clark RE, Broadbent NJ, Squire LR. Impaired remote spatial memory after hippocampal lesions despite extensive training beginning early in life. Hippocampus. 2005;15:340–346. PubMed PMC

Martin SJ, de Hoz L, Morris RG. Retrograde amnesia: Neither partial nor complete hippocampal lesions in rats result in preferential sparing of remote spatial memory, even after reminding. Neuropsychologia. 2005;43:609–624. PubMed

Broadbent NJ, Squire LR, Clark RE. Reversible hippocampal lesions disrupt water maze performance during both recent and remote memory tests. Learn Mem. 2006;13:187–191. PubMed PMC

Teixeira CM, Pomedli SR, Maei HR, Kee N, Frankland PW. Involvement of the anterior cingulate cortex in the expression of remote spatial memory. J Neurosci. 2006;26:7555–7564. PubMed PMC

Alvarez P, Wendelken L, Eichenbaum H. Hippocampal formation lesions impair performance in an odor-odor association task independently of spatial context. Neurobiol Learn Mem. 2002;78:470–476. PubMed

Winocur G, Moscovitch M, Sekeres M. Memory consolidation or transformation: Context manipulation and hippocampal representations of memory. Nat Neurosci. 2007;10:555–557. PubMed

Morris RG, Frey U. Hippocampal synaptic plasticity: Role in spatial learning or the automatic recording of attended experience? Philos Trans R Soc Lond B Biol Sci. 1997;352:1489–1503. PubMed PMC

Kim JJ, Fanselow MS. Modality-specific retrograde amnesia of fear. Science. 1992;256:675–677. PubMed

Matus-Amat P, Higgins EA, Barrientos RM, Rudy JW. The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. J Neurosci. 2004;24:2431–2439. PubMed PMC

Cimadevilla JM, Fenton AA, Bures J. New spatial cognition tests for mice: Passive place avoidance on stable and active place avoidance on rotating arenas. Brain Res Bull. 2001;54:559–563. PubMed

Wesierska M, Dockery C, Fenton AA. Beyond memory, navigation, and inhibition: Behavioral evidence for hippocampus-dependent cognitive coordination in the rat. J Neurosci. 2005;25:2413–2419. PubMed PMC

Kubík S, Stuchlík A, Fenton AA. Evidence for hippocampal role in place avoidance other than merely memory storage. Physiol Res. 2006;55:445–452. PubMed

Telensky P, et al. Enemy avoidance task: A novel behavioral paradigm for assessing spatial avoidance of a moving subject. J Neurosci Methods. 2009;180:29–33. PubMed

Long JM, Kesner RP. The effects of dorsal versus ventral hippocampal, total hippocampal, and parietal cortex lesions on memory for allocentric distance in rats. Behav Neurosci. 1996;110:922–932. PubMed

Long JM, Kesner RP. Effects of hippocampal and parietal cortex lesions on memory for egocentric distance and spatial location information in rats. Behav Neurosci. 1998;112:480–495. PubMed

Muller RU, Kubie JL. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci. 1987;7:1951–1968. PubMed PMC

Rotenberg A, Muller RU. Variable place-cell coupling to a continuously viewed stimulus: Evidence that the hippocampus acts as a perceptual system. Philos Trans R Soc Lond B Biol Sci. 1997;352:1505–1513. PubMed PMC

Knierim JJ, Rao G. Distal landmarks and hippocampal place cells: Effects of relative translation versus rotation. Hippocampus. 2003;13:604–617. PubMed

Leutgeb JK, et al. Progressive transformation of hippocampal neuronal representations in “morphed” environments. Neuron. 2005;48:168–169. PubMed

Trullier O, Shibata R, Mulder AB, Wiener SI. Hippocampal neuronal position selectivity remains fixed to room cues only in rats alternating between place navigation and beacon approach tasks. Eur J Neurosci. 1999;11:4381–4388. PubMed

Ho SA, et al. Hippocampal place cell activity during chasing of a moving object associated with reward in rats. Neuroscience. 2008;157:254–270. PubMed

Zinyuk L, Kubik S, Kaminsky Y, Fenton AA, Bures J. Understanding hippocampal activity by using purposeful behavior: Place navigation induces place cell discharge in both task-relevant and task-irrelevant spatial reference frames. Proc Natl Acad Sci USA. 2000;97:3771–3776. PubMed PMC

Ježek K, et al. Stress-induced out-of-context activation of memory. PLoS Biol. 2010;8:e1000570. PubMed PMC

Segal M, Richter-Levin G, Maggio N. Stress-induced dynamic routing of hippocampal connectivity: A hypothesis. Hippocampus. 2010;20:1332–1338. PubMed

McNaughton N, Gray JA. Anxiolytic action on the behavioural inhibition system implies multiple types of arousal contribute to anxiety. J Affect Disord. 2000;61:161–176. PubMed

Stuchlik A, Rezacova L, Vales K, Bubenikova V, Kubik S. Application of a novel Active Allothetic Place Avoidance task (AAPA) in testing a pharmacological model of psychosis in rats: Comparison with the Morris Water Maze. Neurosci Lett. 2004;366:162–166. PubMed

Paxinos G, Watson CR. The Rat Brain in Stereotaxic Coordinates. 5th Ed. San Diego: Elsevier Academic; 2003.

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace