Neonatal hippocampal lesion alters the functional maturation of the prefrontal cortex and the early cognitive development in pre-juvenile rats

Neurobiology of Learning and Memory

Volumn 97, Issue 4, 2012, Pages 470-481

  Krüger, Hanna Sophie ^a   Brockmann, Marco D ^a   Salamon, Johannes ^a   Ittrich, Harald ^a   Hanganu Opatz, Ileana L ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Anxiety; Development; Hippocampus; NMDA; Oscillatory activity; Prefrontal cortex; Rat pups; Recognition memory

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN DAMAGE; BRAIN MATURATION; COGNITIVE DEVELOPMENT; CONTROLLED STUDY; EXCITOTOXICITY; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; JUVENILE ANIMAL; MALE; MEMORY; MOTOR PERFORMANCE; NERVE CELL NETWORK; NEWBORN; NONHUMAN; PERCEPTION; POSTNATAL DEVELOPMENT; PREFRONTAL CORTEX; RAT; RECOGNITION; TASK PERFORMANCE;

ANIMALS; ANIMALS, NEWBORN; BRAIN WAVES; EXCITATORY AMINO ACID AGONISTS; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; MALE; N-METHYLASPARTATE; NEURAL PATHWAYS; PREFRONTAL CORTEX; RATS; RECOGNITION (PSYCHOLOGY);

EID: 84861191808     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2012.04.001     Document Type: Article

References (51)

1. Ahnaou A., Nayak S., Heylen A., Ashton D., Drinkenburg W.H. Sleep and EEG profile in neonatal hippocampal lesion model of schizophrenia. Physiology & Behavior 2007, 92:461-467.
2. Albasser M.M., Amin E., Iordanova M.D., Brown M.W., Pearce J.M., Aggleton J.P. Perirhinal cortex lesions uncover subsidiary systems in the rat for the detection of novel and familiar objects. European Journal of Neuroscience 2011, 34:331-342.
3. Alleva E., Caprioli A., Laviola G. Litter gender composition affects maternal behavior of the primiparous mouse dam (Mus musculus). Journal of Comparative Psychology 1989, 103:83-87.
4. Anderson M.J., Barnes G.W., Briggs J.F., Ashton K.M., Moody E.W., Joynes R.L., et al. Effects of ontogeny on performance of rats in a novel object-recognition task. Psychological Reports 2004, 94:437-443.
5. Barker G.R., Bird F., Alexander V., Warburton E.C. Recognition memory for objects, place, and temporal order: A disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. Journal of Neuroscience 2007, 27:2948-2957.
6. Barker G.R., Warburton E.C. When is the hippocampus involved in recognition memory?. Journal of Neuroscience 2011, 31:10721-10731.
7. Bertrand J.B., Langlois J.B., Begou M., Volle J., Brun P., d'Amato T., et al. Longitudinal MRI monitoring of brain damage in the neonatal ventral hippocampal lesion rat model of schizophrenia. Hippocampus 2010, 20:264-278.
8. Brockmann M.D., Pöschel B., Cichon N., Hanganu-Opatz I.L. Coupled oscillations mediate directed interactions between prefrontal cortex and hippocampus of the neonatal rat. Neuron 2011, 71:332-347.
9. Brown M.W. Hippocampal and perirhinal functions in recognition memory. Nature Reviews Neuroscience 2008, 9:405.
10. Brown M.W., Aggleton J.P. Recognition memory: What are the roles of the perirhinal cortex and hippocampus?. Nature Reviews Neuroscience 2001, 2:51-61.
11. Brown M.W., Warburton E.C., Aggleton J.P. Recognition memory: Material, processes, and substrates. Hippocampus 2010, 20:1228-1244.
12. Bussey T.J., Duck J., Muir J.L., Aggleton J.P. Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat. Behavioural Brain Research 2000, 111:187-202.
13. Chiba A.A., Kesner R.P., Gibson C.J. Memory for temporal order of new and familiar spatial location sequences: Role of the medial prefrontal cortex. Learning & Memory 1997, 4:311-317.
14. Clark R.E., Zola S.M., Squire L.R. Impaired recognition memory in rats after damage to the hippocampus. Journal of Neuroscience 2000, 20:8853-8860.
15. Clement E.A., Richard A., Thwaites M., Ailon J., Peters S., Dickson C.T. Cyclic and sleep-like spontaneous alternations of brain state under urethane anaesthesia. PLoS One 2008, 3:e2004.
16. Conde F., Maire-Lepoivre E., Audinat E., Crepel F. Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents. The Journal of Comparative Neurology 1995, 352:567-593.
17. Ennaceur A., Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behavioural Brain Research 1988, 31:47-59.
18. Farovik A., Dupont L.M., Arce M., Eichenbaum H. Medial prefrontal cortex supports recollection, but not familiarity, in the rat. Journal of Neuroscience 2008, 28:13428-13434.
19. Feigley D.A., Parsons P.J., Hamilton L.W., Spear N.E. Development of habituation to novel environments in the rat. Journal of Comparative & Physiological Psychology 1972, 79:443-452.
20. File S.E. The ontogeny of exploration in the rat: Habituation and effects of handling. Developmental Psychobiology 1978, 11:321-328.
21. Flechsig P. Developmental (myelogenetic) localization of the cerebral cortex in human subject. Lancet 1901, 1027-1029.
22. Fortin N.J., Agster K.L., Eichenbaum H.B. Critical role of the hippocampus in memory for sequences of events. Nature Neuroscience 2002, 5:458-462.
23. Fox W.M. Reflex-ontogeny and behavioural development of the mouse. Animal Behaviour 1965, 13:234-241.
24. Francois J., Ferrandon A., Koning E., Angst M.J., Sandner G., Nehlig A. Selective reorganization of GABAergic transmission in neonatal ventral hippocampal-lesioned rats. International Journal of Neuropsychopharmacology 2009, 12:1097-1110.
25. Hahn M.E., Lavooy M.J. A review of the methods of studies on infant ultrasound production and maternal retrieval in small rodents. Behavior Genetics 2005, 35:31-52.
26. Hannesson D.K., Howland J.G., Phillips A.G. Interaction between perirhinal and medial prefrontal cortex is required for temporal order but not recognition memory for objects in rats. Journal of Neuroscience 2004, 24:4596-4604.
27. Hasselmo M.E. What is the function of hippocampal theta rhythm? - Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 2005, 15:936-949.
28. Heyser C.J., Chemero A. Novel object exploration in mice: Not all objects are created equal. Behavioural Processes 2012, 89:232-238.
29. Janiesch P.C., Krüger H.S., Pöschel B., Hanganu-Opatz I.L. Cholinergic control in developing prefrontal-hippocampal networks. Journal of Neuroscience 2011, 31:17955-17970.
30. Jay T.M., Witter M.P. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. The Journal of Comparative Neurology 1991, 313:574-586.
31. Kesner R.P., Holbrook T. Dissociation of item and order spatial memory in rats following medial prefrontal cortex lesions. Neuropsychologia 1987, 25:653-664.
32. Kesner R.P., Novak J.M. Serial position curve in rats: Role of the dorsal hippocampus. Science 1982, 218:173-175.
33. Krüger, H. -S., & Hanganu-Opatz, I. L. (2012). Neonatal cholinergic lesion alters the acoustic structure of infant rat vocalization but not the early cognitive development. Developmental Psychobiology. [Epub ahead of print].
34. Langston R.F., Wood E.R. Associative recognition and the hippocampus: Differential effects of hippocampal lesions on object-place, object-context and object-place-context memory. Hippocampus 2010, 20:1139-1153.
35. Lipska B.K., Jaskiw G.E., Weinberger D.R. Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: A potential animal model of schizophrenia. Neuropsychopharmacology 1993, 9:67-75.
36. Mumby D.G., Pinel J.P. Rhinal cortex lesions and object recognition in rats. Behavioral Neuroscience 1994, 108:11-18.
37. Nicolelis M.A., Dimitrov D., Carmena J.M., Crist R., Lehew G., Kralik J.D., et al. Chronic, multisite, multielectrode recordings in macaque monkeys. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:11041-11046.
38. Oh D., Han S., Seo J., Lee J.R., Choi J., Groffen J., et al. Regulation of synaptic Rac1 activity, long-term potentiation maintenance, and learning and memory by BCR and ABR Rac GTPase-activating proteins. Journal of Neuroscience 2010, 30:14134-14144.
39. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego. 4th ed.
40. Pittenger C., Huang Y.Y., Paletzki R.F., Bourtchouladze R., Scanlin H., Vronskaya S., et al. Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 2002, 34:447-462.
41. Reger M.L., Hovda D.A., Giza C.C. Ontogeny of rat recognition memory measured by the novel object recognition task. Developmental Psychobiology 2009, 51:672-678.
42. Rudy J.W., Morledge P. Ontogeny of contextual fear conditioning in rats: Implications for consolidation, infantile amnesia, and hippocampal system function. Behavioral Neuroscience 1994, 108:227-234.
43. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry 1957, 20:11-21.
44. Sharpe R.M. The influence of the sex of litter-mates on subsequent maternal behaviour in Rattus norvegicus. Animal Behaviour 1975, 23:551-559.
45. Siapas A.G., Lubenov E.V., Wilson M.A. Prefrontal phase locking to hippocampal theta oscillations. Neuron 2005, 46:141-151.
46. Steckler T., Drinkenburg W.H., Sahgal A., Aggleton J.P. Recognition memory in rats - II. Neuroanatomical substrates. Progress in Neurobiology 1998, 54:313-332.
47. Steckler T., Sahgal A., Aggleton J.P., Drinkenburg W.H. Recognition memory in rats - III. Neurochemical substrates. Progress in Neurobiology 1998, 54:333-348.
48. Thierry A.M., Gioanni Y., Degenetais E., Glowinski J. Hippocampo-prefrontal cortex pathway: Anatomical and electrophysiological characteristics. Hippocampus 2000, 10:411-419.
49. Tseng K.Y., Lewis B.L., Hashimoto T., Sesack S.R., Kloc M., Lewis D.A., et al. A neonatal ventral hippocampal lesion causes functional deficits in adult prefrontal cortical interneurons. Journal of Neuroscience 2008, 28:12691-12699.
50. Van Eden C.G., Uylings H.B. Cytoarchitectonic development of the prefrontal cortex in the rat. The Journal of Comparative Neurology 1985, 241:253-267.
51. Vertes R.P. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 2006, 142:1-20.