Inactivation of the nucleus reuniens/rhomboid causes a delay-dependent impairment of spatial working memory

Neurobiology of Learning and Memory

Volumn 125, Issue , 2015, Pages 163-167

  Layfield, Dylan M ^a   Patel, Monica ^a   Hallock, Henry ^a   Griffin, Amy L ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Hippocampus; Prefrontal; Reuniens; Rhomboid; Ventral midline thalamus; Working memory

Indexed keywords

MUSCIMOL; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DECISION MAKING; HIPPOCAMPUS; MALE; MEDIAL PREFRONTAL CORTEX; MEMORY DISORDER; NEUROMODULATION; NONHUMAN; RAT; RESPONSE TIME; REUNIENS NUCLEUS; RHOMBOID NUCLEUS; STIMULUS RESPONSE; TASK PERFORMANCE; THALAMUS; WORKING MEMORY; ANIMAL; DRUG EFFECTS; SHORT TERM MEMORY; SPATIAL MEMORY; THALAMUS MIDLINE NUCLEUS;

ANIMALS; GABA-A RECEPTOR AGONISTS; MALE; MEMORY, SHORT-TERM; MIDLINE THALAMIC NUCLEI; MUSCIMOL; RATS; SPATIAL MEMORY;

EID: 84942770511     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2015.09.007     Document Type: Article

References (45)

1. Ainge J.A., van der Meer M.A.A., Langston R.F., Wood E.R. Exploring the role of context-dependent hippocampal activity in spatial alternation behavior. Hippocampus 2007, 17(10):988-1002.
2. Allen T.A., Narayanan N.S., Kholodar-Smith D.B., Zhao Y., Laubach M., Brown T.H. Imaging the spread of reversible brain inactivations using fluorescent muscimol. Journal of Neuroscience Methods 2008, 171(1):30-38.
3. Baddeley A. Working memory: Looking back and looking forward. Nature Reviews Neuroscience 2003, 4:829-837.
4. Bullitt E. Expression of c-Fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. Journal of Comparative Neurology 1990, 296:517-530.
5. Cassel J.C., Pereira V.A., Loureiro M., Cholvin T., Dalrymple-Alford J.C., Vertes R.P. The reuniens and rhomboid nuclei: Neuroanatomy, electrophysiological characteristics and behavioral implications. Progress in Neurobiology 2013, 111:34-52.
6. Chait A., Suaudeau C., De B.R. Extensive brain mapping of calcitonin-induced anorexia. Brain Research Bulletin 1995, 36(5):467-472.
7. Cholvin T., Loureiro M., Cassel R., Cosquer B., Geiger K., De S.N.D., Raingard H., Cassel J.C. The ventral midline thalamus contributes to strategy shifting in a memory task requiring both prefrontal cortical and hippocampal functions. Journal of Neuroscience 2013, 33(20):8772-8783.
8. Churchwell J.C., Kesner R.P. Hippocampal-prefrontal dynamics in spatial working memory: Interactions and independent parallel processing. Behavioural Brain Research 2011, 225:389-395.
9. Colgin L.L. Oscillations and hippocampal-prefrontal synchrony. Current Opinion in Neurobiology 2011, 21:467-474.
10. Czemiawski J., Yoon T., Otto T. Dissociating space and trace in dorsal and ventral hippocampus. Hippocampus 2009, 19(1):20-32.
11. Dostrovsky J.O., Guilbaud G. Nociceptive responses in medial thalamus of the normal and arthritic rat. Pain 1990, 40:93-104.
12. Eichenbaum H., Clegg R.A., Feeley A. Reexamination of functional subdivisions of the rodent prefrontal cortex. Experimental Neurology 1983, 79(2):434-451.
13. Euston D.R., Gruber A.J., McNaughton B.L. The role of medial prefrontal cortex in memory and decision making. Neuron 2012, 76:1057-1070.
14. Ferino F., Thierry A.M., Glowinski J. Anatomical and electrophysiological evidence for a direct projection from ammon's horn to the medial prefrontal cortex in the rat. Experimental Brain Research 1987, 65:421-426.
15. Floresco S.B., Grace A.A. Gating of hippocampal-evoked activity in prefrontal cortical neurons by inputs from the mediodorsal thalamus and ventral tegmental area. Journal of Neuroscience 2003, 23:3930-3943.
16. Floresco S.B., Seamans J.K., Phillips A.G. Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. Journal of Neuroscience 1997, 17:1880-1890.
17. Gholami S., Lambertz D., Hoheisel U., Mense S. Effects on c-Fos expression in the PAG and thalamus by selective input via tetrodotoxin-resistant afferent fibres from muscle and skin. Neuroscience Research 2006, 56:270-278.
18. Gordon J.A. Oscillations and hippocampal-prefrontal synchrony. Current Opinion in Neurobiology 2011, 21:486-491.
19. Hallock H.L., Arreola A.C., Shaw C.L., Griffin A.L. Dissociable roles of the dorsal striatum and dorsal hippocampus in conditional discrimination and spatial alternation T-maze tasks. Neurobiology of Learning and Memory 2013, 100:108-116.
20. Hallock H.L., Wang A., Shaw C.L., Griffin A.L. Transient inactivation of the thalamic nucleus reuniens and rhomboid nucleus produces deficits of a working-memory dependent tactile-visual conditional discrimination task. Behavioral Neuroscience 2013, 127:860-866.
21. Hartley T., Lever C., Burgess N., O'Keefe J. Space in the brain: How the hippocampal formation supports spatial cognition. Philosophical Transactions of the Royal Society of London B: Biological Sciences 2014, 369:20120510. 10.1098/rstb.2012.0510.
22. Hembrook J.R., Mair R.G. Lesions of reuniens and rhomboid thalamic nuclei impair radial maze win-shift performance. Hippocampus 2011, 21(8):815-826.
23. Hembrook J.R., Onos K.D., Mair R.G. Inactivation of ventral midline thalamus produces selective spatial delayed conditional discrimination impairment in the rat. Hippocampus 2012, 22(4):853-860.
24. Ishikawa A., Nakamura S. Convergence and interaction of hippocampal and amygdalar projections within the prefrontal cortex in the rat. Journal of Neuroscience 2003, 23:9987-9995.
25. Ito H.T., Zhang S.J., Witter M.P., Moser E.I., Moser M.B. A prefrontal-thalamo-hippocampal circuit for goal-directed spatial navigation. Nature 2015, 522(7554):50-55.
26. Iwasaki H., Jodo E., Kayama Y., Kawauchi A., Miki T., Koyama Y. Role of the lateral preoptic area and the bed nucleus of stria terminalis in the regulation of penile erection. Brain Research 2010, 1357:70-78.
27. Jankowski M.M., Islam M.N., Wright N.F., Vann S.D., Erichsen J.T., Aggleton J.P., O'Mara S.M. Nucleus reuniens of the thalamus contains head direction cells. Elife 2014, 3.
28. 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. Journal of Comparative Neurology 1991, 313(4):574-586.
29. Jones M.W., Wilson M.A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biology 2005, 3:e402. 10.1371/journal.pbio.0030402.
30. Jung M.W., Qin Y., McNaughton B.L., Barnes C.A. Firing characteristics of deep layer neurons in prefrontal cortex in rats performing spatial working memory tasks. Cerebral Cortex 1998, 8:437-450.
31. Kolb B., Buhrmann K., McDonald R., Sutherland R.J. Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. Cerebral Cortex 1994, 4:664-680.
32. Lee I., Kesner R.P. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. Journal of Neuroscience 2003, 23:1517-1523.
33. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297(5868):681-683.
34. O'Neill P.-K., Gordon J.A., Sigurdsson T. Theta oscillations in the medial prefrontal cortex are modulated by spatial working memory and synchronize with the hippocampus through its ventral subregion. The Journal of Neuroscience 2013, 33:14211-14224.
35. O'Keefe J., Nadel L. The hippocampus as a cognitive map 1978, Clarendon Press, Oxford.
36. Pastalkova E., Itskov V., Amarasingham A., Buzsáki G. Internally generated cell assembly sequences in the rat hippocampus. Science 2008, 321:1322-1327.
37. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2005, Elsevier Academic Press, San Diego. 5th ed.
38. Pereira de Vasconcelos A., Cassel J.-C. The nonspecific thalamus: A place in a wedding bed for making memories last?. Neuroscience and Biobehavioral Reviews 2015, 54:175-196.
39. Squire L.R. Memory and the hippocampus: A synthesis from findings with rats, monkeys and humans. Psychological Review 1992, 99:195-231.
40. Squire L.R. Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory 2004, 82(3):171-177.
41. Urban K.R., Layfield D.M., Griffin A.L. Transient inactivation of the medial prefrontal cortex impairs performance on a working memory-dependent conditional discrimination task. Behavioral Neuroscience 2014, 128(6):639-643.
42. Vertes R.P., Hoover W.B., Do Valle A.C., Sherman A., Rodriguez J.J. Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. Journal of Comparative Neurology 2006, 499(5):768-796.
43. Vertes R.P., Hoover W.B., Szigeti-Buck K., Leranth C. Nucleus reuniens of the midline thalamus: Link between the medial prefrontal cortex and the hippocampus. Brain Research Bulletin 2007, 71(6):601-609.
44. Wilmot C.A., Sullivan A.C., Levin B.E. Effects of diet and obesity on brain alpha1- and alpha2-noradrenergic receptors in the rat. Brain Research 1988, 453:157-166.
45. Xu W., Südhof T.C. A neural circuit for memory specificity and generalization. Science 2013, 339:1290-1295.