Decreasing temperature shifts hippocampal function from memory formation to modulation of hibernation bout duration in syrian hamsters

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 301, Issue 2, 2011, Pages

  Arant, Ryan J ^a   Goo, Marisa S ^a   Gill, Phoebe D ^a   Nguyen, Yen ^a   Watson, Katherine D ^a   Hamilton, Jock S ^a   Horowitz, John M ^a   Horwitz, Barbara A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ascending arousal system; Histamine; Long term depression; Long term potentiation

Indexed keywords

HISTAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AROUSAL; ARTICLE; BRAIN FUNCTION; BRAIN TEMPERATURE; CONTROLLED STUDY; EVOKED RESPONSE; HIBERNATION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYRIAN HAMSTER; TEMPERATURE DEPENDENCE;

ACTION POTENTIALS; ANIMALS; BODY TEMPERATURE REGULATION; COLD TEMPERATURE; CRICETINAE; HIBERNATION; HIPPOCAMPUS; MEMORY; MESOCRICETUS; N-METHYLASPARTATE; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; SYNAPTIC POTENTIALS;

EID: 79961080820     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00016.2011     Document Type: Article

References (42)

1. Axmacher N, Mormann F, Fernandez G, Elger CE, Fell J. Memory formation by neuronal synchronization. Brain Res Brain Res Rev 52: 170-182, 2006.
2. Bear MF, Malenka RC. Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4: 389-399, 1994.
3. Beckman AL, Stanton TL. Changes in CNS responsiveness during hibernation. Am J Physiol 231: 810-816, 1976.
4. Beckman AL, Stanton TL. Properties of the CNS during the state of hibernation. In: Neural Basis of Behavior, edited by Beckman A. Jamaica, NY: Spectrum Publications, 1982.
5. Belousov AB, Vinogradova OS, Pakhotin PI. Paradoxical state-dependent excitability of the medial septal neurons in brain slices of ground squirrel, Citellus undulatus. Neuroscience 38: 599-608, 1990.
6. Boulant JA, Dean JB. Temperature receptors in the central nervous system. Annu Rev Physiol 48: 639-654, 1986.
7. Boulant JA, Demieville HN. Responses of thermosensitive preoptic and septal neurons to hippocampal and brain stem stimulation. J Neurophysiol 40: 1356-1368, 1977.
8. Bronson NW, Piro JB, Hamilton JS, Horowitz JM, Horwitz BA. Temperature modifies potentiation but not depotentiation in bidirectional hippocampal plasticity of Syrian hamsters (Mesocricetus auratus). Brain Res 1098: 61-70, 2006.
9. Carey HV, Andrews MT, Martin SL. Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83: 1153-1181, 2003.
10. Chavez-Noriega LE, Bliss TV, Halliwell JV. The EPSP-spike (E-S) component of long-term potentiation in the rat hippocampal slice is modulated by GABAergic but not cholinergic mechanisms. Neurosci Lett 104: 58-64, 1989.
11. Collingridge GL, Peineau S, Howland JG, Wang YT. Long-term depression in the CNS. Nat Rev Neurosci 11: 459-473, 2010.
12. Dudek SM, Bear MF. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 13: 2910-2918, 1993.
13. Florant GL, Heller HC. CNS regulation of body temperature in euthermic and hibernating marmots (Marmota flaviventris). Am J Physiol Regul Integr Comp Physiol 232: R203-R208, 1977.
14. Fuller P, Sherman D, Pedersen NP, Saper CB, Lu J. Reassessment of the structural basis of the ascending arousal system. J Comp Neurol 519: 933-956, 2011.
15. Green JD, Arduini AA. Hippocampal electrical activity in arousal. J Neurophysiol 17: 533-557, 1954.
16. Heller HC. Hibernation: neural aspects. Annu Rev Physiol 41: 305-321, 1979.
17. Horowitz JM, Horrigan DJ. in Mammals: Central Nervous System Functions. In: Handbook of Physiology Section 4: Environmental Physiology, vol. I, edited by Fregly MJ, and Blatteis CM. New York: Oxford University Press, 1996, p. 533-539.
18. Horwitz BA, Smith RE, Pengelley ET. Estimated heat contribution of brown fat in arousing ground squirrels (Citellus lateralis). Am J Physiol 214: 115-121, 1968.
19. Kilduff TS, Miller JD, Radeke CM, Sharp FR, Heller HC. 14C-2- deoxyglucose uptake in the ground squirrel brain during entrance to and arousal from hibernation. J Neurosci 10: 2463-2475, 1990.
20. Kilduff TS, Sharp FR, Heller HC. [14C]2-deoxyglucose uptake in ground squirrel brain during hibernation. J Neurosci 2: 143-157, 1982.
21. Krelstein MS, Horowitz JM. Tetanus during a high extracellular calcium pulse overrides the block of long-term potentiation seen at 20°C in the hamster hippocampal slice. Brain Res 536: 105-113, 1990.
22. Krelstein MS, Thomas MP, Horowitz JM. Thermal effects on long-term potentiation in the hamster hippocampus. Brain Res 520: 115-122, 1990.
23. Krilowicz BL, Edgar DM, Heller HC. Action potential duration increases as body temperature decreases during hibernation. Brain Res 498: 73-80, 1989.
24. Luthi A, Wikstrom MA, Palmer MJ, Matthews P, Benke TA, Isaac JT, Collingridge GL. Bi-directional modulation of AMPA receptor unitary conductance by synaptic activity. BMC Neurosci 5: 44, 2004.
25. Magarinos AM, McEwen BS, Saboureau M, Pevet P. Rapid and reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters. Proc Natl Acad Sci USA 103: 18775-18780, 2006.
26. Magee J, Hoffman D, Colbert C, Johnston D. Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu Rev Physiol 60: 327-346, 1998.
27. Malenka RC, Nicoll RA. Long-term potentiation-a decade of progress? Science 285: 1870-1874, 1999.
28. Mihailovic LT. Cortical and subcortical electrical activity in hibernation and hypothermia. In: Hibernation and Hypothermia, Perspectives and Challenges, edited by South FE, Hannon J, Willis JR, Pengelley ET, and Alpert NR. Amsterdam: Elsevier, 1972, p. 487-533.
29. Millesi E, Prossinger H, Dittami JP, Fieder M. Hibernation effects on memory in European ground squirrels (Spermophilus citellus). J Biol Rhythms 16: 264-271, 2001.
30. Morrison SF, Nakamura K. Central neural pathways for thermoregulation. Front Biosci 16: 74-104, 2011.
31. Nautiyal KM, Dailey M, Brito N, Brito MN, Harris RB, Bartness TJ, Grill HJ. Energetic responses to cold temperatures in rats lacking forebrain- caudal brain stem connections. Am J Physiol Regul Integr Comp Physiol 295: R789-R798, 2008.
32. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307: 462-465, 1984.
33. Romanovsky AA. Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system. Am J Physiol Regul Integr Comp Physiol 292: R37-R46, 2007.
34. Sallmen T, Lozada AF, Anichtchik OV, Beckman AL, Leurs R, Panula P. Changes in hippocampal histamine receptors across the hibernation cycle in ground squirrels. Hippocampus 13: 745-754, 2003.
35. Sallmen T, Lozada AF, Beckman AL, Panula P. Intrahippocampal histamine delays arousal from hibernation. Brain Res 966: 317-320, 2003.
36. Spangenberger H, Nikmanesh FG, Igelmund P. Long-term potentiation at low temperature is stronger in hippocampal slices from hibernating Turkish hamsters compared to warm-acclimated hamsters and rats. Neurosci Lett 194: 127-129, 1995.
37. Strumwasser F. Regulatory mechanisms, brain activity and behavior during deep hibernation in the squirrel, Citellus beecheyi. Am J Physiol 196: 23-30, 1959.
38. Vinogradova OS. Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11: 578-598, 2001.
39. von der Ohe CG, Darian-Smith C, Garner CC, Heller HC. Ubiquitous and temperature-dependent neural plasticity in hibernators. J Neurosci 26: 10590-10598, 2006.
40. von der Ohe CG, Garner CC, Darian-Smith C, Heller HC. Synaptic protein dynamics in hibernation. J Neurosci 27: 84-92, 2007.
41. Walker JM, Glotzbach SF, Berger RJ, Heller HC. Sleep and hibernation in ground squirrels (Citellus spp): electrophysiological observations. Am J Physiol Regul Integr Comp Physiol 233: R213-R221, 1977.
42. Whitlock JR, Heynen AJ, Shuler MG, Bear MF. Learning induces long-term potentiation in the hippocampus. Science 313: 1093-1097, 2006.