Technical and conceptual considerations for performing and interpreting functional MRI studies in awake rats

Frontiers in Psychiatry

Volumn 2, Issue JUL, 2011, Pages

  Febo, Marcelo ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Anesthesia; Awake rat imaging; Fmri; Motion artifact; Neural circuits; Neuroimaging; Rats; Stress

Indexed keywords

ACCLIMATIZATION; BEHAVIOR CHANGE; BEHAVIOR DISORDER; BOLD SIGNAL; BRAIN REGION; CELL ACTIVITY; CELL INTERACTION; CHRONIC STRESS; DEPRESSION; ELECTROENCEPHALOGRAM; EVOKED SOMATOSENSORY RESPONSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HEMODYNAMICS; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMOBILIZATION STRESS; NERVE CELL; NONHUMAN; REVIEW; SENSORY STIMULATION; SPIKE WAVE; STEADY STATE; STIMULUS RESPONSE; WAKEFULNESS;

EID: 84866877636     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2011.00043     Document Type: Review

References (146)

1. Angenstein, F., Krautwald, K., and Sche-ich, H. (2011). The current functional state of local neuronal circuits controls the magnitude of a BOLDresponsetoincoming stimuli. Neuroimage 50, 1364-1375.
2. Aoki, I., Tanaka, C., Takegami, T., Ebisu, T., Umeda, M., Fukunaga, M., Fukuda, K., Silva, A. C., Koretsky, A. P., and Naruse, S. (2002). Dynamic activity-induced manganese-dependent contrast magnetic resonance imaging (DAIM MRI). Magn. Reson. Med. 48, 927-933.
3. Attwell, D., and Iadecola, C. (2002). The neural basis of functional brain imaging signals. Trends Neurosci. 25, 621-625.
4. Austin, V. C., Blamire, A. M., Allers, K. A., Sharp, T., Styles, P., Matthews, P. M., and Sibson, N. R. (2005). Confounding effects of anesthesia on functional activation in rodent brain: a study of halothane and alpha-chloralose anesthesia. Neu-roimage 24, 92-100.
5. Bandettini, P. A., and Wong, E. C. (1997). A hypercapnia-based normalization method for improved spatial localization of human brain activation with fMRI. NMR Biomed. 10, 197-203.
6. Bandettini, P. A., Wong, E. C., Hinks, R. S., Tikofsky, R. S., and Hyde, J. S. (1992). Time course EPI of human brain function during task activation. Magn. Reson. Med. 25, 390-397.
7. Barnum, C. J., Blandino, P. Jr., and Deak, T. (2007). Adaptation in the corticosterone and hyperther-mic responses to stress following repeated stressor exposure. J. Neu-roendocrinol. 19, 632-642.
8. Bartels, A., and Zeki, S. (2004). The neural correlates of maternal and romantic love. Neuroimage 21, 1155-1166.
9. Belda, X., Fuentes, S., Nadal, R., and Armario, A. (2008). A single exposure to immobilization causes long-lasting pituitary-adrenal and behavioral sensitization to mild stressors. Horm. Behav. 54, 654-661.
10. Bhattacharyya, P. K., and Lowe, M. J. (2004). Cardiac-induced physiologic noise in tissue is a direct observationof cardiac-induced fluctuations. Magn. Reson. Imaging 22, 9-13.
11. Blyton, D. M., Sullivan, C. E., and Edwards, N. (2002). Lactation is associated with an increase in slow-wave sleep in women. J. Sleep Res. 11, 297-303.
12. Breiter, H. C., Gollub, R. L., Weisskoff, R. M., Kennedy, D. N., Makris, N., Berke,J. D., Goodman,J. M., Kantor, H. L., Gastfriend, D. R., Riorden, J. P., Mathew, R. T., Rosen, B. R., and Hyman, S. E. (1997). Acute effects of cocaineon human brain activityand emotion. Neuron 19, 591-611.
13. Brevard, M. E., Duong, T. Q., King, J. A., and Ferris, C. F. (2003). Changes in MRI signal intensity during hyper-capnic challenge under conscious and anesthetized conditions. Magn. Reson. Imaging 21, 995-1001.
14. Brevard, M. E., Meyer, J. S., Harder, J. A., and Ferris, C. F. (2006). Imaging brain activity in conscious monkeys following oral MDMA ("ecstasy"). Magn. Reson. Imaging 24, 707-714.
15. Briski, K. P., and Sylvester, P. W. (1987). Effects of repetitive daily acute stress on pituitary LH and prolactin release during exposure to the same stressor or a second novel stress. Psychoneu-roendocrinology 12, 429-437.
16. Buxton, R. B. (2002). Introduction to Functional Magnetic Resonance Imaging: Principles and Techniques. New York: Cambridge University Press.
17. Buzsaki, G., Kaila, K., and Raichle, M. (2007). Inhibition and brain work. Neuron 56, 771-783.
18. Chang, J.Y., Janak,P. H., and Woodward, D. J. (1998). Comparison of meso-corticolimbic neuronal responses during cocaine and heroin self-administration infreely moving rats. J. Neurosci. 18, 3098-3115.
19. Chen, W., Shields, J., Huang, W., and King, J. A. (2009). Female fear: influence of estrus cycle on behavioral response and neuronal activation. Behav. Brain Res. 201, 8-13.
20. Chen, W., Tenney, J., Kulkarni, P., and King, J. A. (2007). Imaging unconditioned fear response with manganese-enhanced MRI (MEMRI). Neuroimage 37, 221-229.
21. Chin, C. L., Fox, G. B., Hradil, V. P., Osinski, M. A., Mcgaraughty, S. P., Skoubis, P. D., Cox, B. F., and Luo, Y. (2006). Pharmacological MRI in awake rats reveals neural activity in area postrema and nucleus tractus solitarius: relevance as a potential biomarker for detecting drug-induced emesis. Neuroimage 33, 1152-1160.
22. Chin, C. L., Upadhyay, J., Marek, G. J., Baker, S. J., Zhang, M., Mezler, M., Fox, G. B., and Day, M. (2011). Awake rat pharmacological magnetic resonance imaging as a translational pharmacody-namic biomarker:metabotropicglu-tamate 2/3 agonist modulation of ketamine-induced blood oxygena-tion level dependence signals. J. Pharmacol. Exp. Ther. 336, 709-715.
23. Cohen, E. R., Ugurbil, K., and Kim, S. G. (2002). Effect of basal conditions on the magnitude and dynamics of the blood oxygenation level-dependent fMRI response. J. Cereb. Blood Flow Metab. 22, 1042-1053.
24. Davis, T. L., Kwong, K. K., Weisskoff, R. M., and Rosen, B. R. (1998). Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc. Natl. Acad. Sci. U.S.A. 95, 1834-1839.
25. Desai, M., Kahn, I., Knoblich, U., Bernstein, J., Atallah, H., Yang, A., Kopell, N., Buckner, R. L., Graybiel, A. M., Moore, C. I., and Boyden, E. S. (2011). Mapping brain networks in awake mice using combined optical neural control and fMRI. J. Neuro-physiol. 105, 1393-1405.
26. Desalvo, M. N., Schridde, U., Mishra, A. M., Motelow, J. E., Purcaro, M. J., Danielson, N., Bai, X., Hyder, F., and Blumenfeld, H. (2011). Focal BOLD fMRI changes in bicuculline-induced tonic-clonic seizures in the rat. Neuroimage 50, 902-909.
27. Dhabhar, F. S., Mcewen, B. S., and Spencer, R. L. (1997). Adaptation to prolonged or repeated stress - comparison between rat strains showing intrinsic differences in reactivity to acute stress. Neuroen-docrinology 65, 360-368.
28. Doty, F. D., Entzminger, G., Kulkarni, J., Pamarthy, K., and Staab, J. P. (2007). Radio frequency coil technology for small-animal MRI. NMR. Biomed. 20, 304-325.
29. Douglas, R., Markram, H., and Martin, K. (2004). "Neocortex," in The Synaptic Organization of the Brain, ed. G. M. Sheperd, 5th Edn (New York: Oxford University Press), 499-558.
30. Dubois-Dauphin, M., Armstrong, W. E., Tribollet, E., and Dreifuss, J. J. (1985). Somatosensory systems and the milk-ejection reflex in the rat. II. The effects of lesions in the ventroposterior thalamic complex, dorsal columns and lateral cervical nucleus-dorsolateral funiculus. Neuroscience 15, 1131-1140.
31. Duong, T. Q., Silva, A. C., Lee, S. P., and Kim,S.G. (2000).Functional MRI of calcium-dependent synaptic activity: cross correlation with CBF and BOLD measurements. Magn. Reson. Med. 43, 383-392.
32. Duong, T. Q., Yacoub, E., Adriany, G., Hu, X., Ugurbil, K., and Kim, S. G. (2003). Microvascular BOLD contribution at 4 and 7 T in the human brain: gradient-echo and spin-echo fMRI with suppression of blood effects. Magn. Reson. Med. 49, 1019-1027.
33. Eger, E. I. II, and Johnson, B. H. (1987). Rates of awakening from anesthesia with I-653, halothane, isoflu-rane, and sevoflurane: a test of the effect of anesthetic concentration and duration in rats. Anesth. Analg. 66, 977-982.
34. Einhorn, L. C., Johansen, P. A., and White, F. J. (1988). Electrophysiolog-ical effects of cocaine in the mesoac-cumbens dopamine system: studies in the ventral tegmental area. J. Neurosci. 8, 100-112.
35. Febo, M., and Ferris, C. F. (2007). Development of cocaine sensiti-zation before pregnancy affects subsequent maternal retrieval of pups and prefrontal cortical activity during nursing. Neuroscience 148, 400-412.
36. Febo, M., Ferris, C. F., and Segarra, A. C. (2005a). Estrogen influences cocaine-induced blood oxygen level-dependent signal changes in female rats. J. Neurosci. 25, 1132-1136.
37. Febo, M., Numan, M., and Ferris, C. F. (2005b). Functional magnetic resonance imaging shows oxy-tocin activates brain regions associated with mother-pup bonding during suckling. J. Neurosci. 25, 11637-11644.
38. Febo, M., Segarra, A. C., Nair, G., Schmidt, K., Duong, T. Q., and Ferris, C. F. (2004a). The neural consequences of repeated cocaine exposure revealed by functional MRI in awake rats. Neuropsychopharma-cology 30, 936-943.
39. Febo, M., and Pira, A. S. (2011). Increased BOLD activation to predator stressor in subiculum and mid-brain of amphetamine-sensitized maternal rats. Brain Res. 1382, 118-127.
40. Febo, M., Segarra, A. C., Tenney, J. R., Brevard, M. E., Duong, T. Q., and Ferris, C. F. (2004b). Imaging cocaine-induced changes in the mesocorticolimbic dopamin-ergic system of conscious rats. J. Neurosci. Methods 139, 167-176.
41. Febo, M., Stolberg, T. L., Numan, M., Bridges, R. S., Kulkarni, P., and Ferris, C. F. (2008). Nursing stimulation is more than tactile sensation: it is a multisensory experience. Horm. Behav. 54, 330-339.
42. Ferris, C. F., Febo, M., Luo, F., Schmidt, K., Brevard, M., Harder, J. A., Kulka-rni, P., Messenger, T., and King, J. A. (2006). Functional magnetic resonance imaginginconscious animals: a new tool in behavioural neuro-science research. J. Neuroendocrinol. 18, 307-318.
43. Ferris, C. F., Kulkarni, P., Sullivan, J. M. Jr., Harder, J. A., Messenger, T. L., and Febo, M. (2005). Pup suckling is more rewarding than cocaine: evidence from functional magnetic resonance imaging and three-dimensional computational analysis. J. Neurosci. 25, 149-156.
44. Ferris, C. F., Snowdon, C. T., King, J. A., Duong, T. Q., Ziegler, T. E., Ugur-bil, K., Ludwig, R., Schultz-Darken, N. J., Wu, Z., Olson, D. P., Sullivan Jr, J. M., Tannenbaum, P. L., and Vaughan, J. T. (2001). Functional imaging of brain activity in conscious monkeys responding to sexually arousing cues. Neuroreport 12, 2231-2236.
45. Ferris, C. F., Snowdon, C. T., King, J. A., Sullivan, J. M. Jr., Ziegler, T. E., Olson, D. P., Schultz-Darken, N. J., Tannenbaum, P. L., Ludwig, R., Wu, Z., Einspanier, A., Vaughan, J. T., and Duong, T. Q. (2004). Activation of neural pathways associated with sexual arousal in non-human primates. J. Magn. Reson. Imaging 19, 168-175.
46. Ferris, C. F., Stolberg, T., Kulkarni, P., Murugavel, M., Blanchard, R., Blan-chard, D. C., Febo, M., Brevard, M., and Simon, N. G. (2008). Imaging the neural circuitry and chemical control of aggressive motivation. BMC Neurosci. 9, 111. doi: 10.1186/1471-2202-9-111
47. Fox, P. T., and Raichle, M. E. (1986). Focal physiological uncoupling of cerebral blood flow and oxida-tive metabolism during somatosen-sory stimulation in human subjects. Proc. Natl. Acad. Sci. U.S.A. 83, 1140-1144.
48. Fox, P. T., Raichle, M. E., Mintun, M. A., and Dence, C. (1988). Nonoxidative glucose consumption during focal physiologic neural activity. Science 241, 462-464.
49. Freire, L., and Mangin, J. F. (2001). Motion correction algorithms may create spurious brain activations in the absence of subject motion. Neu-roimage 14, 709-722.
50. Garcia, A., Marti, O., Valles, A., Dal-Zotto, S., and Armario, A. (2000). Recovery of the hypothalamic-pituitary-adrenal response to stress. Effect of stress intensity, stress duration and previous stress exposure. Neuroendocrinology 72, 114-125.
51. Genovese, C. R., Lazar, N. A., and Nichols, T. (2002). Thresholding of statistical maps in functional neu-roimaging using the false discovery rate. Neuroimage 15, 870-878.
52. Girotti, M., Pace, T. W., Gaylord, R. I., Rubin, B. A., Herman, J. P., and Spencer, R. L. (2006). Habituation to repeated restraint stress is associated with lack of stress-induced c-fos expression in primary sensory processing areas of the rat brain. Neuroscience 138, 1067-1081.
53. Goense, J. B., and Logothetis, N. K. (2006). Laminar specificity in monkey V1 using high-resolution SE-fMRI. Magn. Reson. Imaging 24, 381-392.
54. Goense, J. B., and Logothetis, N. K. (2008). Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr. Biol. 18, 631-640.
55. Gollub, R. L., Breiter, H. C., Kantor, H., Kennedy,D.,Gastfriend,D.,Mathew, R. T., Makris, N., Guimaraes, A., Riorden, J., Campbell, T., Foley, M., Hyman, S. E., Rosen, B., and Weis-skoff, R. (1998). Cocaine decreases cortical cerebral blood flow but does not obscure regional activation in functional magnetic resonance imaging in human subjects. J. Cereb. Blood Flow Metab. 18, 724-734.
56. Greenberg, D. S., Houweling, A. R., and Kerr, J. N. (2008). Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat. Neurosci. 11, 749-751.
57. Haleem, D. J. (1996). Adaptation to repeated restraint stress in rats: failure of ethanol-treated rats to adapt in the stress schedule. Alcohol Alcohol. 31, 471-477.
58. Hammer, R. P. Jr., Pires, W. S., Markou, A., and Koob, G. F. (1993). Withdrawal following cocaine self-administration decreases regional cerebral metabolic rate in critical brain reward regions. Synapse 14, 73-80.
59. Harel, N., Lee, S. P., Nagaoka, T., Kim, D. S., and Kim, S. G. (2002). Origin of negative blood oxygenation level-dependent fMRI signals. J. Cereb. Blood Flow Metab. 22, 908-917.
60. Hartikainen, K. M., Rorarius, M., Perakyla, J. J., Laippala, P. J., and Jantti, V. (1995). Cortical reactivity during isoflurane burst-suppression anesthesia. Anesth. Analg. 81, 1223-1228.
61. Huttunen, J. K., Grohn, O., and Penttonen, M. (2008). Coupling between simultaneously recorded BOLD response and neuronal activity in the rat somatosensory cortex. Neuroimage 39, 775-785.
62. Hyder, F., Rothman, D. L., and Shulman, R. G. (2002). Total neuroenerget-ics support localized brain activity: implications for the interpretation of fMRI. Proc. Natl. Acad. Sci. U.S.A. 99, 10771-10776.
63. Imas, O. A., Ropella, K. M., Ward, B. D., Wood, J. D., and Hudetz, A. G. (2005). Volatile anesthetics enhance flash-induced gamma oscillations in rat visual cortex. Anesthesiology 102, 937-947.
64. Imas, O. A., Ropella, K. M., Wood, J. D., and Hudetz, A. G. (2004). Halothane augments event-related gamma oscillations in rat visual cortex. Neuroscience 123, 269-278.
65. Imperato, A., Mele, A., Scrocco, M. G., and Puglisi-Allegra, S. (1992). Chronic cocaine alters limbic extracellular dopamine. Neurochemical basis for addiction. Eur. J. Pharmacol. 212, 299-300.
66. Kalivas, P. W., and Duffy, P. (1993). Time course of extracellular dopamine and behavioral sensitization to cocaine. I. Dopamine axon terminals. J. Neurosci. 13, 266-275.
67. Kant, G. J., Eggleston, T., Landman-Roberts, L., Kenion, C. C., Driver, G. C., and Meyerhoff, J. L. (1985). Habituation to repeated stress is stressor specific. Pharmacol. Biochem. Behav. 22, 631-634.
68. Kasischke, K. A., Vishwasrao, H. D., Fisher, P. J., Zipfel, W. R., and Webb, W. W. (2004). Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305, 99-103.
69. Kaufman, M. J.,Levin, J. M., Maas, L. C., Rose, S. L., Lukas, S. E., Mendelson, J. H., Cohen, B. M., and Renshaw, P. F. (1998). Cocaine decreases relative cerebral blood volume in humans: a dynamic susceptibility contrast magnetic resonance imaging study. Psychopharmacology (Berl.) 138, 76-81.
70. Kennerley, A. J., Berwick, J., Martin-dale, J., Johnston, D., Papadakis, N., and Mayhew, J. E. (2005). Concurrent fMRI and optical measures for the investigation of the hemo-dynamic response function. Magn. Reson. Med. 54, 354-365.
71. Kim, D. S., Duong, T. Q., and Kim, S. G. (2000). High-resolution mapping of iso-orientation columns by fMRI. Nat. Neurosci. 3, 164-169.
72. King, J. A., Garelick, T. S., Brevard, M. E., Chen, W., Messenger, T. L., Duong, T. Q., and Ferris, C. F. (2005). Procedure for minimizing stress for fMRI studies in conscious rats. J. Neurosci. Methods 148, 154-160.
73. Krishnan, V., and Nestler, E. J. (2008). The molecular neurobiology of depression. Nature 455, 894-902.
74. Lahti, K. M., Ferris, C. F., Li, F., Sotak, C. H., and King, J. A. (1998). Imaging brain activity in conscious animals using functional MRI. J. Neurosci. Methods 82, 75-83.
75. Lahti, K. M., Ferris, C. F., Li, F., Sotak, C. H., and King, J. A. (1999). Comparison of evoked cortical activity in conscious and propofol-anesthetized rats using functional MRI. Magn. Reson. Med. 41, 412-416.
76. Lee, A., Li, M., Watchus, J., and Fleming, A. S. (1999). Neuroanatomical basis of maternal memory in post-partum rats: selective role for the nucleus accumbens. Behav. Neurosci. 113, 523-538.
77. Lee, S. P., Duong, T. Q., Yang, G., Iadecola, C., and Kim, S. G. (2001). Relative changes of cerebral arterial and venous blood volumes during increased cerebral blood flow: implications for BOLD fMRI. Magn. Reson. Med. 45, 791-800.
78. Li, S. J., Biswal, B., Li, Z., Risinger, R., Rainey, C., Cho, J. K., Salmeron, B. J., and Stein, E. A. (2000). Cocaine administration decreases functional connectivity in human primary visual and motor cortex as detected by functional MRI. Magn. Reson. Med. 43, 45-51.
79. Liang,Z.,King,J.,and Zhang,N.Uncov-ering intrinsic connectional architecture of functional networks in awake rat brain. (2011). J. Neurosci. 31, 3776-3783.
80. Lin, S. H., Miyata, S., Matsunaga, W., Kawarabayashi, T., Nakashima, T., and Kiyohara, T. (1998). Metabolic mapping of the brain in pregnant, parturient and lactating rats using fos immunohistochemistry. Brain Res. 787, 226-236.
81. Lincoln, D. W., Hentzen, K., Hin, T., Van Der Schoot, P., Clarke, G., and Summerlee,A. J. (1980). Sleep: a prerequisite for reflex milk ejection in the rat. Exp. Brain Res. 38, 151-162.
82. Liu, X., Zhu, X. H., Zhang, Y., and Chen, W. (2011). Neural origin of spontaneous hemodynamic fluctuations in rats under burst-suppression anesthesia condition. Cereb. Cortex 21, 374-384.
83. Logothetis, N. K. (2008). What we can do and what we cannot do with fMRI. Nature 453, 869-878.
84. Logothetis, N. K., Pauls, J., Augath, M., Trinath, T., and Oeltermann, A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature 412, 150-157.
85. London, E. D., Wilkerson, G., Goldberg, S. R., and Risner, M. E. (1986). Effects of L-cocaine on local cerebral glucose utilization in the rat. Neurosci. Lett. 68, 73-78.
86. Lonstein, J. S., Simmons, D. A., Swann, J. M., and Stern, J. M. (1998). Fore-brain expression of c-fos due to active maternal behaviour in lactat-ing rats. Neuroscience 82, 267-281.
87. Lonstein, J. S., and Stern, J. M. (1997). Somatosensory contributions to c-fos activation within the caudal peri-aqueductal gray of lactating rats: effects of perioral, rooting, and suckling stimuli from pups. Horm. Behav. 32, 155-166.
88. Lorberbaum, J. P., Newman, J. D., Hor-witz, A. R., Dubno, J. R., Lydiard, R. B., Hamner, M. B., Bohning, D. E., and George, M. S. (2002). A potential role for thalamocingulate circuitry in human maternal behavior. Biol. Psychiatry 51, 431-445.
89. Lu, H., Xi, Z. X., Gitajn, L., Rea, W., Yang, Y., and Stein, E. A. (2007). Cocaine-induced brain activation detected by dynamic manganese-enhanced magnetic resonance imaging (MEMRI). Proc. Natl. Acad. Sci. U.S.A. 104, 2489-2494.
90. Ludwig, R., Bodgdanov, G., King, J., Allard, A., and Ferris, C. F. (2004). A dual RF resonator system for high-field functional magnetic resonance imaging of small animals. J. Neu-rosci. Methods 132, 125-135.
91. Malonek, D., Dirnagl, U., Lindauer, U., Yamada, K., Kanno, I., and Grin-vald, A. (1997). Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow,oxygenation, and volume changes following sensory stimulation. Proc. Natl. Acad. Sci. U.S.A. 94, 14826-14831.
92. Malonek, D., and Grinvald, A. (1996). Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science 272, 551-554.
93. Mandeville, J. B., Jenkins, B. G., Kosof-sky, B. E., Moskowitz, M. A., Rosen, B. R., and Marota, J. J. (2001). Regional sensitivity and coupling of BOLD and CBV changes dur ing stimulation of rat brain. Magn. Reson. Med. 45, 443-447.
94. Marota, J. J., Mandeville, J. B., Weis-skoff, R. M., Moskowitz, M. A., Rosen, B. R., and Kosofsky, B. E. (2000). Cocaine activation discriminates dopaminergic projections by temporal response: an fMRI study in Rat. Neuroimage 11, 13-23.
95. Martin, C., Martindale, J., Berwick, J., and Mayhew, J. (2006). Investigating neural-hemodynamic coupling and the hemodynamic response function in the awake rat. Neuroimage 32, 33-48.
96. Masamoto, K., Fukuda, M., Vazquez, A., and Kim, S. G. (2009). Dose-dependent effect of isoflurane on neurovascular coupling in rat cerebral cortex. Eur. J. Neurosci. 30, 242-250.
97. Melia, K. R., Ryabinin, A. E., Schroeder, R., Bloom, F. E., and Wilson, M. C. (1994). Induction and habitua-tion of immediate early gene expres sion in rat brain by acute and repeated restraint stress. J. Neurosci. 14, 5929-5938.
98. Miller, M. J., Chen, N. K., Li, L., Tom, B., Weiss, C., Disterhoft, J. F., and Wyr-wicz, A. M. (2003). fMRI of the conscious rabbit during unilateral classical eyeblink conditioning reveals bilateral cerebellar activation. J. Neu-rosci. 23, 11753-11758.
99. Mogenson, G. J., and Yang, C. R. (1991). The contribution of basal forebrain to limbic-motor integration and the mediation of motivation to action. Adv. Exp. Med. Biol. 295, 267-290.
100. Nadasdy, Z., Csicsvari, J., Penttonen, M., Hetke, J., Wise, K., and Buzsaki, G. (1998). "Extracellular recording and analysis of neuronal activity: from single cells to ensembles," in Neuronal Ensembles: Strategies for Recording and Decoding, 1st Edn, eds H. Eichenbaum and J. L. Davis (New York: Wiley-Liss), 17-56.
101. Naert, G., Ixart, G., Maurice, T., Tapia-Arancibia, L., and Givalois, L. (2011). Brain-derived neurotrophic factor and hypothalamic-pituitary-adrenal axis adaptation processes in a depressive-like state induced by chronic restraint stress. Mol. Cell. Neurosci. 46, 55-66.
102. Nairismagi, J., Pitkanen, A., Narki-lahti, S., Huttunen, J., Kauppinen, R. A., and Grohn, O. H. (2006). Manganese-enhanced magnetic resonance imaging of mossy fiber plasticity in vivo. Neuroimage 30, 130-135.
103. Nakao, Y., Itoh, Y., Kuang, T. Y., Cook, M., Jehle, J., and Sokoloff, L. (2001). Effects of anesthesia on functional activation of cerebral blood flow and metabolism. Proc. Natl. Acad. Sci. U.S.A. 98, 7593-7598.
104. Nitschke, J. B., Nelson, E. E., Rusch, B. D., Fox, A. S., Oakes, T. R., and Davidson, R. J. (2004). Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants. Neuroimage 21, 583-592.
105. Ogawa, S., Lee, T. M., Kay, A. R., and Tank, D. W. (1990). Brain magnetic resonance imaging with contrast dependent on blood oxygena-tion. Proc. Natl. Acad. Sci. U.S.A. 87, 9868-9872.
106. Ogawa, S., Tank, D. W., Menon, R., Eller-mann, J. M., Kim, S. G., Merkle, H., and Ugurbil, K. (1992). Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc. Natl. Acad. Sci. U.S.A. 89, 5951-5955.
107. Parry, T. J., and Mcelligott, J. G. (1993). A method for restraining awake rats using head immobilization. Physiol. Behav. 53, 1011-1015.
108. Parsons, L. H., Koob, G. F., and Weiss, F. (1996). Extracellular serotonin is decreased in the nucleus accumbens during withdrawal from cocaine self-administration. Behav. Brain Res. 73, 225-228.
109. Pauling, L., and Coryell, C. D. (1936). The magnetic properties and structure of hemoglobin, oxyhemoglo-bin and carbonmonoxyhemoglobin. Proc. Natl. Acad. Sci. U.S.A. 22, 210-216.
110. Pautler, R. G., Mongeau, R., and Jacobs, R. E. (2003). In vivo trans-synaptic tract tracing from the murine striatum and amygdala utilizing manganese enhanced MRI (MEMRI). Magn. Reson. Med. 50, 33-39.
111. Paxinos, G., and Watson, C. (1997). The Rat Brain in Stereotaxic Coordinates. Boston: Academic Press.
112. Peeters, R. R., Tindemans, I., De Schut-ter, E., and Van Der Linden, A. (2001). Comparing BOLD fMRI signal changes in the awake and anesthetized rat during electrical forepaw stimulation. Magn. Reson. Imaging 19, 821-826.
113. Peeters, R. R., and Van Der Linden, A. (2002). A data post-processing protocol for dynamic MRI data to discriminate brain activity from global physiological effects. Magn. Reson. Imaging 20, 503-510.
114. Pierzchala, K., and Van Loon, G. R. (1990). Plasma native and peptidase-derivable Met-enkephalin responses to restraint stress in rats. Adaptation to repeated restraint. J. Clin. Invest. 85, 861-873.
115. Porrino, L. J., Domer, F. R., Crane, A. M., and Sokoloff, L. (1988). Selective alterations in cerebral metabolism within the mesocorticolim-bic dopaminergic system produced by acute cocaine administration in rats. Neuropsychopharmacology 1, 109-118.
116. Poser, B. A., and Norris, D. G. (2007). Fast spin echo sequences for BOLD functional MRI. MAGMA 20,11-17.
117. Purdon, P. L., and Weisskoff, R. M. (1998). Effect of temporal autocorrelation due to physiological noise and stimulus paradigm on voxel-level false-positive rates in fMRI. Hum. Brain Mapp. 6, 239-249.
118. Sachdev, R. N., Champney, G. C., Lee, H., Price, R. R., Pickens, D. R. III, Morgan,V. L., Stefansic, J. D., Melzer, P., and Ebner, F. F. (2003). Experimental model for functional magnetic resonance imaging of somatic sensory cortex in the unanesthetized rat. Neuroimage 19, 742-750.
119. Saleem, K. S., Pauls, J. M., Augath, M., Trinath, T., Prause, B. A., Hashikawa, T., and Logothetis, N. K. (2002). Magnetic resonance imaging of neu-ronal connections in the macaque monkey. Neuron 34, 685-700.
120. Schmidt, K. F., Febo, M., Shen, Q., Luo, F., Sicard,K. M., Ferris,C. F., Stein, E. A., and Duong, T. Q. (2006). Hemo-dynamic and metabolic changes induced by cocaine in anesthetized rat observed with multimodal functional MRI. Psychopharmacology (Berl.) 185, 479-486.
121. Schridde, U., Khubchandani, M., Motelow, J. E., Sanganahalli, B. G., Hyder, F., and Blumenfeld, H. (2008). Negative BOLD with large increases in neuronal activity. Cereb. Cortex 18, 1814-1827.
122. Seehafer, J. U., Kalthoff, D., Farr, T. D., Wiedermann, D., and Hoehn, M. (2011).Noincreaseofthebloodoxy-genation level-dependent functional magnetic resonance imaging signal with higher field strength: implications for brain activation studies. J. Neurosci. 30, 5234-5241.
123. Sheth, S. A., Nemoto, M., Guiou, M., Walker, M., Pouratian, N., and Toga, A. W. (2004). Linear and nonlinear relationships between neuronal activity, oxygen metabolism, and hemodynamicresponses. Neuron 42, 347-355.
124. Shmuel, A., Augath, M., Oeltermann, A., and Logothetis, N. K. (2006). Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat. Neurosci. 9, 569-577.
125. Shmuel, A., Yacoub, E., Pfeuffer, J., Van De Moortele, P. F., Adriany, G., Hu, X., and Ugurbil,K. (2002). Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron 36, 1195-1210.
126. Sicard, K., Shen, Q., Brevard, M. E., Sullivan, R., Ferris, C. F., King, J. A., and Duong, T. Q. (2003). Regional cerebral blood flow and BOLD responses in conscious and anesthetized rats under basal and hypercapnic conditions: implications for functional MRI studies. J. Cereb. Blood Flow Metab. 23, 472-481.
127. Silva, A. C., and Koretsky, A. P. (2002). Laminar specificity of functional MRI onset times during somatosen-sory stimulation in rat. Proc. Natl. Acad. Sci. U.S.A. 99, 15182-15187.
128. Stamp, J., and Herbert, J. (2001). Cor-ticosterone modulates autonomic responses and adaptation of central immediate-early gene expression to repeated restraint stress. Neu-roscience 107, 465-479.
129. Stein, E. A., and Fuller, S. A. (1992). Selective effects of cocaine on regional cerebral blood flow in the rat. J. Pharmacol. Exp. Ther. 262, 327-334.
130. Stein, E. A., and Fuller, S. A. (1993). Cocaine's time action profile on regional cerebral blood flow in the rat. Brain Res. 626, 117-126.
131. Stern, J. M., and Johnson, S. K. (1990). Ventral somatosensory determinants of nursing behavior in Norway rats. I. Effects of variations in the quality and quantity of pup stimuli. Physiol. Behav. 47, 993-1011.
132. Stern, J. M., Yu, Y. L., and Crockett, D. P. (2002). Dorsolateral columns of the spinal cord are necessary for both suckling-induced neuroen-docrine reflexes and the kyphotic nursing posture in lactating rats. Brain Res. 947, 110-121.
133. Strathearn, L., Li, J., Fonagy, P., and Montague, P. R. (2008). What's in a smile? Maternal brain responses to infant facial cues. Pediatrics 122, 40-51.
134. Tasker, J. G., Theodosis, D. T., and Poulain, D. A. (1986). Afferent projections from the mammary glands to the spinal cord in the lac-tating rat - I. A neuroanatomi-cal study using the transganglionic transport of horseradish peroxidase-wheatgerm agglutinin. Neuroscience 19, 495-509.
135. Thompson, J. K., Peterson, M. R., and Freeman, R. D. (2003). Single-neuron activity and tissue oxygena-tion in the cerebral cortex. Science 299, 1070-1072.
136. Tian, P., Teng, I. C., May, L. D., Kurz, R., Lu, K., Scadeng, M., Hill-man, E. M., De Crespigny, A. J., D'arceuil, H. E., Mandeville, J. B., Marota, J. J., Rosen, B. R., Liu, T. T., Boas, D. A., Buxton, R. B., Dale, A. M., and Devor, A. (2011). Cortical depth-specific microvascu-lar dilation underlies laminar differences in blood oxygenation level-dependent functional MRI signal. Proc. Natl. Acad. Sci. U.S.A. 107, 15246-15251.
137. Tornatzky, W., and Miczek, K. A. (1993). Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol. Behav. 53, 983-993.
138. Ugurbil, K., Adriany, G., Andersen, P., Chen, W., Garwood, M., Gruetter, R., Henry, P. G., Kim, S. G., Lieu, H., Tkac, I., Vaughan, T., Van De Moortele, P. F., Yacoub, E., and Zhu, X. H. (2003). Ultrahigh field magnetic resonance imaging and spec-troscopy. Magn. Reson. Imaging 21, 1263-1281.
139. Walsh, C. J., Fleming, A. S., Lee, A., and Magnusson, J. E. (1996). The effects of olfactory and somatosen-sory desensitization on Fos-like immunoreactivity in the brains of pup-exposed postpartum rats. Behav. Neurosci. 110, 134-153.
140. Wang, K., Van Meer, M. P., Van Der Marel, K., Van Der Toorn, A., Xu, L., Liu, Y., Viergever, M. A., Jiang, T., and Dijkhuizen, R. M. (2011). Temporal scaling properties and spatial synchronization of spontaneous blood oxygenation level-dependent (BOLD) signal fluctuations in rat sensorimotor network at different levels of isoflu-rane anesthesia. NMR Biomed. 24, 61-67.
141. Williams, K. A., Magnuson, M., Majeed, W., Laconte, S. M., Peltier, S. J., Hu, X., and Keilholz, S. D. (2011). Comparison of alpha-chloralose, medetomidine and isoflurane anesthesia for functional connectivity mapping in the rat. Magn. Reson. Imaging 28, 995-1003.
142. Xerri, C., Stern, J. M., and Merzenich, M. M. (1994). Alterations of the cortical representation of the rat ven-trum induced by nursing behavior. J. Neurosci. 14, 1710-1721.
143. Xi, Z. X., Wu, G., Stein, E. A., and Li, S. J. (2004). Opiate tolerance by heroin self-administration: an fMRI study in rat. Magn. Reson. Med. 52, 108-114.
144. Ye, Y., Zhuo, Y., Xue, R., and Zhou, X. J. (2011). BOLD fMRI using a modified HASTE sequence. Neuroimage 49, 457-466.
145. Yu, X., Wadghiri, Y. Z., Sanes, D. H., and Turnbull, D. H. (2005). In vivo auditory brain mapping in mice with Mn-enhanced MRI. Nat. Neurosci.8, 961-968.
146. Zhang, N., Rane, P., Huang, W., Liang, Z., Kennedy, D., Frazier, J. A., and King, J. (2011). Mapping resting-state brain networks in conscious animals. J. Neurosci. Methods 189, 186-196