Brain tissue oxygen amperometry in behaving rats demonstrates functional dissociation of dorsal and ventral hippocampus during spatial processing and anxiety

European Journal of Neuroscience

Volumn 33, Issue 2, 2011, Pages 322-337

  McHugh, Stephen B ^a   Fillenz, Marianne ^a   Lowry, John P ^b   Rawlins, J Nicolas P ^a   Bannerman, David M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Constant potential amperometry; Dorsal hippocampus; Oxygen; Tissue oxygen voltammetry; Ventral hippocampus

Indexed keywords

AMPEROMETRY; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; DORSAL HIPPOCAMPUS; EXPERIMENTAL TEST; HIPPOCAMPUS; IN VIVO STUDY; LOCOMOTION; MALE; MAZE TEST; NEOPHOBIA; NONHUMAN; NONREM SLEEP; OXYGEN TISSUE LEVEL; PRIORITY JOURNAL; RAT; REM SLEEP; SPATIAL MEMORY; TASK PERFORMANCE; VENTRAL HIPPOCAMPUS; WAKEFULNESS;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; ELECTROCHEMICAL TECHNIQUES; HIPPOCAMPUS; HUMANS; MALE; MAZE LEARNING; MEMORY; NEUROPSYCHOLOGICAL TESTS; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; SPACE PERCEPTION;

EID: 78651447230     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07497.x     Document Type: Article

References (78)

1. Attwell, D. & Iadecola, C. (2002) The neural basis of functional brain imaging signals. Trends Neurosci., 25, 621-625.
2. Bannerman, D.M., Yee, B.K., Good, M.A., Heupel, M.J., Iversen, S.D. & Rawlins, J.N. (1999) Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav. Neurosci., 113, 1170-1188.
3. Bannerman, D.M., Deacon, R.M., Offen, S., Friswell, J., Grubb, M. & Rawlins, J.N. (2002) Double dissociation of function within the hippocampus: spatial memory and hyponeophagia. Behav. Neurosci., 116, 884-901.
4. Bannerman, D.M., Rawlins, J.N., McHugh, S.B., Deacon, R.M., Yee, B.K., Bast, T., Zhang, W.N., Pothuizen, H.H. & Feldon, J. (2004) Regional dissociations within the hippocampus - memory and anxiety. Neurosci. Biobehav. Rev., 28, 273-283.
5. Bazzu, G., Puggioni, G.G., Dedola, S., Calia, G., Rocchitta, G., Migheli, R., Desole, M.S., Lowry, J.P., O' Neill, R.D. & Serra, P.A. (2009) Real-time monitoring of brain tissue oxygen using a miniaturized biotelemetric device implanted in freely moving rats. Anal. Chem., 81, 2235-2241.
6. Canteras, N.S. & Swanson, L.W. (1992) Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J. Comp. Neurol., 324, 180-194.
7. Challis, R.E. & Kitney, R.I. (1990) Bio-medical signal-processing (in 4 parts) .1. Time-domain methods. Med. Biol. Eng. Compu., 28, 509-524.
8. Cheng, S. & Frank, L.M. (2008) New experiences enhance coordinated neural activity in the hippocampus. Neuron, 57, 303-313.
9. Crawley, J. & Goodwin, F.K. (1980) Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol. Biochem. Behav., 13, 167-170.
10. Csicsvari, J., O'Neill, J., Allen, K. & Senior, T. (2007) Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration. Eur. J. Neurosci., 26, 704-716.
11. Czurko, A., Hirase, H., Csicsvari, J. & Buzsaki, G. (1999) Sustained activation of hippocampal pyramidal cells by 'space clamping' in a running wheel. Eur. J. Neurosci., 11, 344-352.
12. Davis, M. & Shi, C. (1999) The extended amygdala: are the central nucleus of the amygdala and the bed nucleus of the stria terminalis differentially involved in fear versus anxiety? Ann. N Y Acad. Sci., 877, 281-291.
13. Faraci, F.M. & Breese, K.R. (1993) Nitric oxide mediates vasodilatation in response to activation of N-methyl-D-aspartate receptors in brain. Circ. Res., 72, 476-480.
14. Fergus, A. & Lee, K.S. (1997) Regulation of cerebral microvessels by glutamatergic mechanisms. Brain Res., 754, 35-45.
15. Foster, T.C., Castro, C.A. & McNaughton, B.L. (1989) Spatial selectivity of rat hippocampal neurons: dependence on preparedness for movement. Science, 244, 1580-1582.
16. Gray, J.A. (1982). The Neuropsychology of Anxiety, 1st edn. Oxford University Press, Oxford.
17. Gray, J.A. & McNaughton, N. (2000). The Neuropsychology of Anxiety, 2nd Edn. Oxford University Press, Oxford.
18. van Groen, T. & Wyss, J.M. (1990) Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J. Comp. Neurol., 302, 515-528.
19. Gueorguieva, R. & Krystal, J.H. (2004) Move over ANOVA: progress in analyzing repeated-measures data and its reflection in papers published in the Archives of General Psychiatry. Arch. Gen. Psychiatry, 61, 310-317.
20. Hartley, T., Maguire, E.A., Spiers, H.J. & Burgess, N. (2003) The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron, 37, 877-888.
21. Hasler, G., Fromm, S., Alvarez, R.P., Luckenbaugh, D.A., Drevets, W.C. & Grillon, C. (2007) Cerebral blood flow in immediate and sustained anxiety. J. Neurosci., 27, 6313-6319.
22. Hitchman, M.L. (1978) Measurement of Dissolved Oxygen. John Wiley, New York.
23. Hock, B.J.. Jr & Bunsey, M.D. (1998) Differential effects of dorsal and ventral hippocampal lesions. J. Neurosci., 18, 7027-7032.
24. Howell, D.C. (2010) Statistical Methods for Psychology, 7th Edition. Wadsworth, Cengage Learning, Belmont.
25. Jung, M.W., Wiener, S.I. & McNaughton, B.L. (1994) Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci., 14, 7347-7356.
26. Kane, D.A. & O' Neill, R.D. (1998) Major differences in the behaviour of carbon paste and carbon fibre electrodes in a protein-lipid matrix: implications for voltammetry in vivo. Analyst, 123, 2899-2903.
27. Keppel, G. (1982) Design and Analysis: a Researcher's Handbook, 2nd Edn. Prentice Hall, London.
28. Kjelstrup, K.G., Tuvnes, F.A., Steffenach, H.A., Murison, R., Moser, E.I. & Moser, M.B. (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc. Natl. Acad. Sci. USA, 99, 10825-10830.
29. Kjelstrup, K.B., Solstad, T., Brun, V.H., Hafting, T., Leutgeb, S., Witter, M.P., Moser, E.I. & Moser, M.B. (2008) Finite scale of spatial representation in the hippocampus. Science, 321, 140-143.
30. Krettek, J.E. & Price, J.L. (1977) Projections from the amygdaloid complex and adjacent olfactory structures to the entorhinal cortex and to the subiculum in the rat and cat. J. Comp. Neurol., 172, 723-752.
31. Kumaran, D. & Maguire, E.A. (2005) The human hippocampus: cognitive maps or relational memory? J. Neurosci., 25, 7254-7259.
32. Laird, N.M. & Ware, J.H. (1982) Random-effects models for longitudinal data. Biometrics, 38, 963-974.
33. Lauritzen, M. (2005) Reading vascular changes in brain imaging: is dendritic calcium the key? Nat. Rev. Neurosci., 6, 77-85.
34. Logothetis, N.K. (2008) What we can do and what we cannot do with fMRI. Nature, 453, 869-878.
35. Logothetis, N.K., Pauls, J., Augath, M., Trinath, T. & Oeltermann, A. (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature, 412, 150-157.
36. Louie, K. & Wilson, M.A. (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron, 29, 145-156.
37. Louis, R.P., Lee, J. & Stephenson, R. (2004) Design and validation of a computer-based sleep-scoring algorithm. J. Neurosci. Methods, 133, 71-80.
38. Lovick, T.A., Brown, L.A. & Key, B.J. (1999) Neurovascular relationships in hippocampal slices: physiological and anatomical studies of mechanisms underlying flow-metabolism coupling in intraparenchymal microvessels. Neuroscience, 92, 47-60.
39. Lowry, J.P., Boutelle, M.G. & Fillenz, M. (1997) Measurement of brain tissue oxygen at a carbon past electrode can serve as an index of increases in regional cerebral blood flow. J. Neurosci. Methods, 71, 177-182.
40. Lowry, J.P., Griffin, K., McHugh, S.B., Lowe, A.S., Tricklebank, M. & Sibson, N.R. (2010) Real-time electrochemical monitoring of brain tissue oxygen: a surrogate for functional magnetic resonance imaging in rodents. Neuroimage, 52, 549-555.
41. Maguire, E.A., Frackowiak, R.S. & Frith, C.D. (1997) Recalling routes around london: activation of the right hippocampus in taxi drivers. J. Neurosci., 17, 7103-7110.
42. Maguire, E.A., Burgess, N., Donnett, J.G., Frackowiak, R.S., Frith, C.D. & O'Keefe, J. (1998) Knowing where and getting there: a human navigation network. Science, 280, 921-924.
43. Masamoto, K., Vazquez, A., Wang, P. & Kim, S.G. (2008) Trial-by-trial relationship between neural activity, oxygen consumption, and blood flow responses. Neuroimage, 40, 442-450.
44. Mathiesen, C., Caesar, K., Akgoren, N. & Lauritzen, M. (1998) Modification of activity-dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex. J. Physiol., 512 (Pt 2), 555-566.
45. Matsuura, T. & Kanno, I. (2001) Quantitative and temporal relationship between local cerebral blood flow and neuronal activation induced by somatosensory stimulation in rats. Neurosci. Res., 40, 281-290.
46. Maurer, A.P., Vanrhoads, S.R., Sutherland, G.R., Lipa, P. & McNaughton, B.L. (2005) Self-motion and the origin of differential spatial scaling along the septo-temporal axis of the hippocampus. Hippocampus, 15, 841-852.
47. McHugh, S.B., Deacon, R.M., Rawlins, J.N. & Bannerman, D.M. (2004) Amygdala and ventral hippocampus contribute differentially to mechanisms of fear and anxiety. Behav. Neurosci., 118, 63-78.
48. Mintun, M.A., Lundstrom, B.N., Snyder, A.Z., Vlassenko, A.G., Shulman, G.L. & Raichle, M.E. (2001) Blood flow and oxygen delivery to human brain during functional activity: theoretical modeling and experimental data. Proc. Natl. Acad. Sci. USA, 98, 6859-6864.
49. Moser, M.B., Moser, E.I., Forrest, E., Andersen, P. & Morris, R.G. (1995) Spatial learning with a minislab in the dorsal hippocampus. Proc. Natl. Acad. Sci. U S A, 92, 9697-9701.
50. Nitz, D. & McNaughton, B. (2004) Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. J. Neurophysiol., 91, 863-872.
51. Norup Nielsen, A. & Lauritzen, M. (2001) Coupling and uncoupling of activity-dependent increases of neuronal activity and blood flow in rat somatosensory cortex. J. Physiol., 533, 773-785.
52. O' Neill, R.D. (1993) Sensor-tissue interactions in neurochemical analysis with carbon paste electrodes in vivo. Analyst, 118, 433-438.
53. O' Neill, R.D., Grunewald, R.A., Fillenz, M. & Albery, W.J. (1982) Linear sweep voltammetry with carbon paste electrodes in the rat striatum. Neuroscience, 7, 1945-1954.
54. Offenhauser, N., Thomsen, K., Caesar, K. & Lauritzen, M. (2005) Activity-induced tissue oxygenation changes in rat cerebellar cortex: interplay of postsynaptic activation and blood flow. J. Physiol., 565, 279-294.
55. Ormonde, D.E. & O'Neill, R.D. (1989) Altered response of carbon paste electrodes after contact with brain-tissue - implications for modified electrode use in vivo. J. Electroanal. Chem., 261, 463-469.
56. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th Edn. Academic Press, New York.
57. Pentkowski, N.S., Blanchard, D.C., Lever, C., Litvin, Y. & Blanchard, R.J. (2006) Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. Eur. J. Neurosci., 23, 2185-2196.
58. Piepho, H.P., Buchse, A. & Emrich, K. (2003) A hitchhiker's guide to mixed models for randomized experiments. J. Agron. Crop Sci., 189, 310-322.
59. Pikkarainen, M., Ronkko, S., Savander, V., Insausti, R. & Pitkanen, A. (1999) Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J. Comp. Neurol., 403, 229-260.
60. Poe, G.R., Nitz, D.A., McNaughton, B.L. & Barnes, C.A. (2000) Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res., 855, 176-180.
61. Pothuizen, H.H., Zhang, W.N., Jongen- Relo, A.L., Feldon, J. & Yee, B.K. (2004) Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: a within-subject, within-task comparison of reference and working spatial memory. Eur. J. Neurosci., 19, 705-712.
62. Powers, W.J., Hirsch, I.B. & Cryer, P.E. (1996) Effect of stepped hypoglycemia on regional cerebral blood flow response to physiological brain activation. Am. J. Physiol., 270, H554-H559.
63. Risold, P.Y. & Swanson, L.W. (1996) Structural evidence for functional domains in the rat hippocampus. Science, 272, 1484-1486.
64. Rodgers, R.J., Haller, J., Holmes, A., Halasz, J., Walton, T.J. & Brain, P.F. (1999) Corticosterone response to the plus-maze: high correlation with risk assessment in rats and mice. Physiol. Behav., 68, 47-53.
65. Rolls, E.T., Cahusac, P.M., Feigenbaum, J.D. & Miyashita, Y. (1993) Responses of single neurons in the hippocampus of the macaque related to recognition memory. Exp. Brain Res., 93, 299-306.
66. Sanderson, D.J., McHugh, S.B., Good, M.A., Sprengel, R., Seeburg, P.H., Rawlins, J.N. & Bannerman, D.M. (2010) Spatial working memory deficits in GluA1 AMPA receptor subunit knockout mice reflect impaired short-term habituation: evidence for Wagner's dual-process memory model. Neuropsychologia, 48, 2303-2315.
67. Shephard, R.A. & Estall, L.B. (1984) Anxiolytic actions of chlordiazepoxide determine its effects on hyponeophagia in rats. Psychopharmacology (Berl.), 82, 343-347.
68. Silva, A.C., Lee, S.P., Iadecola, C. & Kim, S.G. (2000) Early temporal characteristics of cerebral blood flow and deoxyhemoglobin changes during somatosensory stimulation. J. Cereb. Blood Flow Metab., 20, 201-206.
69. Smith, A.J., Blumenfeld, H., Behar, K.L., Rothman, D.L., Shulman, R.G. & Hyder, F. (2002) Cerebral energetics and spiking frequency: the neurophysiological basis of fMRI. Proc. Natl. Acad. Sci. USA, 99, 10765-10770.
70. Taylor, R.J. & Humffray, A.A. (1975) Electrochemical studies on glassy carbon electrodes .3. Oxygen reduction in solutions of low pH]pH less-than 10). J. Electroanal. Chem., 64, 85-94.
71. Thompson, J.K., Peterson, M.R. & Freeman, R.D. (2003) Single-neuron activity and tissue oxygenation in the cerebral cortex. Science, 299, 1070-1072.
72. Thompson, J.K., Peterson, M.R. & Freeman, R.D. (2005) Separate spatial scales determine neural activity-dependent changes in tissue oxygen within central visual pathways. J. Neurosci., 25, 9046-9058.
73. Vanderkooi, J.M., Erecinska, M. & Silver, I.A. (1991) Oxygen in mammalian tissue: methods of measurement and affinities of various reactions. Am. J. Physiol., 260, C1131-C1150.
74. Vann, S.D., Brown, M.W., Erichsen, J.T. & Aggleton, J.P. (2000) Fos imaging reveals differential patterns of hippocampal and parahippocampal subfield activation in rats in response to different spatial memory tests. J. Neurosci., 20, 2711-2718.
75. Viswanathan, A. & Freeman, R.D. (2007) Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity. Nat. Neurosci., 10, 1308-1312.
76. Yamaguchi, S., Hale, L.A., D'Esposito, M. & Knight, R.T. (2004) Rapid prefrontal-hippocampal habituation to novel events. J. Neurosci., 24, 5356-5363.
77. Zheng, Y., Martindale, J., Johnston, D., Jones, M., Berwick, J. & Mayhew, J. (2002) A model of the hemodynamic response and oxygen delivery to brain. Neuroimage, 16, 617-637.
78. Zimmerman, J.B. & Wightman, R.M. (1991) Simultaneous electrochemical measurements of oxygen and dopamine in vivo. Anal. Chem., 63, 24-28.