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PLOS ONE  2012 

Brain Processing of Biologically Relevant Odors in the Awake Rat, as Revealed by Manganese-Enhanced MRI

DOI: 10.1371/journal.pone.0048491

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Abstract:

Background So far, an overall view of olfactory structures activated by natural biologically relevant odors in the awake rat is not available. Manganese-enhanced MRI (MEMRI) is appropriate for this purpose. While MEMRI has been used for anatomical labeling of olfactory pathways, functional imaging analyses have not yet been performed beyond the olfactory bulb. Here, we have used MEMRI for functional imaging of rat central olfactory structures and for comparing activation maps obtained with odors conveying different biological messages. Methodology/Principal Findings Odors of male fox feces and of chocolate flavored cereals were used to stimulate conscious rats previously treated by intranasal instillation of manganese (Mn). MEMRI activation maps showed Mn enhancement all along the primary olfactory cortex. Mn enhancement elicited by male fox feces odor and to a lesser extent that elicited by chocolate odor, differed from that elicited by deodorized air. This result was partly confirmed by c-Fos immunohistochemistry in the piriform cortex. Conclusion/Significance By providing an overall image of brain structures activated in awake rats by odorous stimulation, and by showing that Mn enhancement is differently sensitive to different stimulating odors, the present results demonstrate the interest of MEMRI for functional studies of olfaction in the primary olfactory cortex of laboratory small animals, under conditions close to natural perception. Finally, the factors that may cause the variability of the MEMRI signal in response to different odor are discussed.

References

[1]  Johnson BA, Ong J, Leon M (2010) Glomerular activity patterns evoked by natural odor objects in the rat olfactory bulb are related to patterns evoked by major odorant components. J Comp Neurol 518: 1542–1555.
[2]  Sharp FR, Kauer JS, Shepherd GM (1977) Laminar analysis of 2-deoxyglucose uptake in olfactory bulb and olfactory cortex of rabbit and rat. J Neurophysiol 40: 800–813.
[3]  Woo CC, Hingco EE, Johnson BA, Leon M (2007) Broad activation of the glomerular layer enhances subsequent olfactory responses. Chem Senses 32: 51–55.
[4]  Datiche F, Roullet F, Cattarelli M (2001) Expression of Fos in the piriform cortex after acquisition of olfactory learning: an immunohistochemical study in the rat. Brain Res Bull 55: 95–99.
[5]  Funk D, Amir S (2000) Enhanced fos expression within the primary olfactory and limbic pathways induced by an aversive conditioned odor stimulus. Neuroscience 98: 403–406.
[6]  Guthrie KM, Anderson AJ, Leon M, Gall C (1993) Odor-induced increases in c-fos mRNA expression reveal an anatomical “unit” for odor processing in olfactory bulb. Proc Natl Acad Sci U S A 90: 3329–3333.
[7]  Illig KR, Haberly LB (2003) Odor-evoked activity is spatially distributed in piriform cortex. J Comp Neurol 457: 361–373.
[8]  Schwarz J, Burguet J, Rampin O, Fromentin G, Andrey P, et al. (2010) Three-dimensional macronutrient-associated Fos expression patterns in the mouse brainstem. PLoS ONE 5: e8974.
[9]  Charpak S, Mertz J, Beaurepaire E, Moreaux L, Delaney K (2001) Odor-evoked calcium signals in dendrites of rat mitral cells. Proc Natl Acad Sci U S A 98: 1230–1234.
[10]  Petzold GC, Albeanu DF, Sato TF, Murthy VN (2008) Coupling of neural activity to blood flow in olfactory glomeruli is mediated by astrocytic pathways. Neuron 58: 897–910.
[11]  Stettler DD, Axel R (2009) Representations of odor in the piriform cortex. Neuron 63: 854–864.
[12]  F?rster S, Vaitl A, Teipel SJ, Yakushev I, Mustafa M, et al. (2010) Functional representation of olfactory impairment in early Alzheimer’s disease. J Alzheimers Dis 22: 581–591.
[13]  Qureshy A, Kawashima R, Imran MB, Sugiura M, Goto R, et al. (2000) Functional mapping of human brain in olfactory processing: a PET study. J Neurophysiol 84: 1656–1666.
[14]  Royet JP, Koenig O, Gregoire MC, Cinotti L, Lavenne F, et al. (1999) Functional anatomy of perceptual and semantic processing for odors. J Cogn Neurosci 11: 94–109.
[15]  Savic I, Berglund H (2010) Androstenol–a steroid derived odor activates the hypothalamus in women. PLoS ONE 5: e8651.
[16]  Schepkin VD, Brey WW, Gor’kov PL, Grant SC (2010) Initial in vivo rodent sodium and proton MR imaging at 21.1 T. Magn Reson Imaging 28: 400–407.
[17]  Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS (1992) Time course EPI of human brain function during task activation. Magn Reson Med 25: 390–397.
[18]  Kwong KK, Belliveau JW, Chesler DA, Goldberg IE, Weisskoff RM, et al. (1992) Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci U S A 89: 5675–5679.
[19]  Ogawa S, Lee T-M (1990) Magnetic resonance imaging of blood vessels at high fields: In vivo and in vitro measurements and image simulation. Magn Reson Med 16: 9–18.
[20]  Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, et al. (2005) Breakdown of cortical effective connectivity during sleep. Science 309: 2228–2232.
[21]  Shulman RG, Rothman DL, Hyder F (1999) Stimulated changes in localized cerebral energy consumption under anesthesia. Proc Natl Acad Sci U S A 96: 3245–3250.
[22]  Alkire MT, Hudetz AG, Tononi G (2008) Consciousness and anesthesia. Science 322: 876–880.
[23]  Ferris CF, Febo M, Luo F, Schmidt K, Brevard M, et al. (2006) Functional magnetic resonance imaging in conscious animals: a new tool in behavioural neuroscience research. J Neuroendocrinol 18: 307–318.
[24]  Chen W, Shields J, Huang W, King JA (2009) Female fear: influence of estrus cycle on behavioral response and neuronal activation. Behav Brain Res 201: 8–13.
[25]  Febo M, Shields J, Ferris CF, King JA (2009) Oxytocin modulates unconditioned fear response in lactating dams: an fMRI study. Brain Res 1302: 183–193.
[26]  Febo M, Pira AS (2011) Increased BOLD activation to predator stressor in subiculum and midbrain of amphetamine-sensitized maternal rats. Brain Res 1382: 118–127.
[27]  Huang W, Heffernan ME, Li Z, Zhang N, Overstreet DH, et al. (2011) Fear induced neuronal alterations in a genetic model of depression: an fMRI study on awake animals. Neurosci Lett 489: 74–78.
[28]  Kulkarni P, Stolberg T, Sullivanjr JM, Ferris CF (2012) Imaging evolutionarily conserved neural networks: preferential activation of the olfactory system by food-related odor. Behav Brain Res 230: 201–207.
[29]  Martin C (2007) Anaesthetic use in animal models for neuroimaging. Neuroimage 38: 1–2; discussion 3–4.
[30]  Silva AC, Lee JH, Aoki I, Koretsky AP (2004) Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed 17: 532–543.
[31]  Lin YJ, Koretsky AP (1997) Manganese ion enhances T1-weighted MRI during brain activation: an approach to direct imaging of brain function. Magn Reson Med 38: 378–388.
[32]  Chuang KH, Koretsky AP, Sotak CH (2009) Temporal changes in the T1 and T2 relaxation rates (DeltaR1 and DeltaR2) in the rat brain are consistent with the tissue-clearance rates of elemental manganese. Magn Reson Med 61: 1528–1532.
[33]  Chuang KH, Lee JH, Silva AC, Belluscio L, Koretsky AP (2009) Manganese enhanced MRI reveals functional circuitry in response to odorant stimuli. Neuroimage 44: 363–372.
[34]  Pautler RG, Koretsky AP (2002) Tracing odor-induced activation in the olfactory bulbs of mice using manganese-enhanced magnetic resonance imaging. Neuroimage 16: 441–448.
[35]  De Groof G, Gwinner H, Steiger S, Kempenaers B, Van der Linden A (2010) Neural correlates of behavioural olfactory sensitivity changes seasonally in European starlings. PLoS ONE 5: e14337.
[36]  Crossgrove J, Zheng W (2004) Manganese toxicity upon overexposure. NMR Biomed 17: 544–553.
[37]  Lehallier B, Coureaud G, Maurin Y, Bonny JM (2012) Effects of manganese injected into rat nostrils: implications for in vivo functional study of olfaction using MEMRI. Magn Reson Imaging 30: 62–69.
[38]  Lehallier B, Andrey P, Maurin Y, Bonny JM (2011) Iterative algorithm for spatial and intensity normalization of MEMRI images. Application to tract-tracing of rat olfactory pathways. Magn Reson Imaging 29: 1304–1316.
[39]  Vernet-Maury E, Le Magnen J, Chanel J (1968) Emotional behavior of rats; influence of the odor of a predator and a non-predator. C R Acad Sci Hebd Seances Acad Sci D 267: 331–334.
[40]  Schroeder BE, Binzak JM, Kelley AE (2001) A common profile of prefrontal cortical activation following exposure to nicotine- or chocolate-associated contextual cues. Neuroscience 105: 535–545.
[41]  Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Amsterdam; Boston: Academic Press/Elsevier.
[42]  Chuang KH, Koretsky AP (2009) Accounting for nonspecific enhancement in neuronal tract tracing using manganese enhanced magnetic resonance imaging. Magn Reson Imaging 27: 594–600.
[43]  Cross DJ, Minoshima S, Anzai Y, Flexman JA, Keogh BP, et al. (2004) Statistical mapping of functional olfactory connections of the rat brain in vivo. Neuroimage 23: 1326–1335.
[44]  Pautler RG, Silva AC, Koretsky AP (1998) In vivo neuronal tract tracing using manganese-enhanced magnetic resonance imaging. Magn Reson Med 40: 740–748.
[45]  Chuang KH, Belluscio L, Koretsky AP (2010) In vivo detection of individual glomeruli in the rodent olfactory bulb using manganese enhanced MRI. Neuroimage 49: 1350–1356.
[46]  Sosulski DL, Lissitsyna Bloom M, Cutforth T, Axel R, Datta SR (2011) Distinct representations of olfactory information in different cortical centres. Nature 472: 213–216.
[47]  Morgan JI, Cohen DR, Hempstead JL, Curran T (1987) Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237: 192–197.
[48]  Rampin O, Bellier C, Maurin Y (2012) Electrophysiological responses of rat olfactory tubercle neurons to biologically relevant odours. Eur J Neurosci 35: 97–105.
[49]  Van der Linden A, Van Camp N, Ramos-Cabrer P, Hoehn M (2007) Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition. NMR Biomed 20: 522–545.
[50]  Nordh?y W, Anthonsen HW, Bruvold M, Brurok H, Skarra S, et al. (2004) Intracellular manganese ions provide strong T1 relaxation in rat myocardium. Magn Reson Med 52: 506–514.
[51]  Arevian AC, Kapoor V, Urban NN (2008) Activity-dependent gating of lateral inhibition in the mouse olfactory bulb. Nat Neurosci 11: 80–87.
[52]  Lledo PM, Gheusi G, Vincent JD (2005) Information processing in the mammalian olfactory system. Physiol Rev 85: 281–317.
[53]  Wilson DA, Sullivan RM (2011) Cortical processing of odor objects. Neuron 72: 506–519.
[54]  Woods RP, Grafton ST, Holmes CJ, Cherry SR, Mazziotta JC (1998) Automated image registration: I. General methods and intrasubject, intramodality validation. J Comput Assist Tomogr 22: 139–152.

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