Neural processing of a cocaine-associated odor cue revealed by functional MRI in awake rats
Open accessAbstract
Using an olfactory conditioning procedure, brain stimulation reward threshold measurements, and functional magnetic resonance imaging (fMRI), we investigated brain stimulation reward threshold change and fMRI neural activation in response to a cocaine-associated odor cue. In the first brain stimulation experiment, over 10 days of rate-frequency curve-shift testing, rats were administered intravenous cocaine (1.0mg/kg) paired with a contextual cue of peppermint odor previously placed in the operant chamber or they were given vehicle treatment (no cocaine) in the presence of no olfactory cue. Following a 14-day drug-free rest period, rats were again given the rate-frequency curve-shift threshold test with or without the odor cue. In a second experiment, rats were similarly conditioned with a peppermint odor but with intraperitoneally delivered cocaine (10mg/kg). After a 14 day rest period, rats were imaged on a 7-T MRI for their blood oxygen level dependent (BOLD) in response to the cocaine-paired peppermint odor versus an unpaired neutral lemon odor. In the brain stimulation experiment, expected significant reward threshold shifts were produced by cocaine and, importantly, about half that level of shift was produced by the paired contextual olfactory cue. In the fMRI experiment, the insular cortex showed a significantly greater BOLD activation in cocaine-treated versus saline-treated animals to the olfactory cue, but not with the unpaired lemon scent. These data are in agreement with previous studies suggesting a role of the insular cortex in attributing reward value (positive or negative) to conditioned odor stimuli.
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Functional MRI responses to drug-associated cues in adult rodents after chronic cocaine exposure show remarkable faithfulness to human and other primate fMRI changes, including elevated responses in the dorsal STR, NAc, mPFC, and insular cortex.
“Functional MRI responses to drug-associated cues in adult rodents after chronic cocaine exposure show remarkable faithfulness to human and other primate fMRI changes, including elevated responses in the dorsal STR, NAc, mPFC, and insular cortex (Johnson et al., 2013, Liu et al., 2013).”
From Sensitive periods of substance abuse: Early risk for the transition to dependence (2017) · cites this paper as Johnson et al., 2013
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Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Koob, G. F., & Volkow, N. D. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.110 · Cited by 5,340 · see citing works
Thresholding of statistical maps in functional neuroimaging using the false discovery rate
Genovese, C. R., Lazar, N. A., & Nichols, T. (2002) · NeuroImage · doi:10.1006/nimg.2001.1037 · Cited by 4,923 · see citing works
The Synaptic Organization of the Brain
(2004) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195159561.001.1 · Cited by 3,550 · see citing works
Differential projections of the infralimbic and prelimbic cortex in the rat
Vertes, R. P. (2004) · Synapse · doi:10.1002/syn.10279 · Cited by 1,550 · see citing works
Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat
Hoover, W. B., & Vertes, R. P. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0150-4 · Cited by 1,365 · see citing works
Damage to the insula disrupts addiction to cigarette smoking
Naqvi, N. H., Rudrauf, D., Damasio, H., & Bechara, A. (2007) · Science · doi:10.1126/science.1135926 · Cited by 1,245 · see citing works
Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction
Volkow, N. D., Wang, G.-J., Telang, F., Fowler, J. S., Logan, J., Childress, A.-R., Jayne, M., Ma, Y., & Wong, C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1544-06.2006 · Cited by 1,164 · see citing works
Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli
Garavan, H., Pankiewicz, J., Bloom, A., Cho, J.-K., Sperry, L., Ross, T. J., Salmeron, B. J., Risinger, R., Kelley, D., & Stein, E. A. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.11.1789 · Cited by 931 · see citing works
Brain circuitry and the reinstatement of cocaine-seeking behavior
Kalivas, P., & McFarland, K. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1393-2 · Cited by 613 · see citing works
Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making
Clark, L., Bechara, A., Damasio, H., Aitken, M. R. F., Sahakian, B. J., & Robbins, T. W. (2008) · Brain · doi:10.1093/brain/awn066 · Cited by 613 · see citing works
Price, J. L. (1973) · The Journal of Comparative Neurology · doi:10.1002/cne.901500105 · Cited by 530 · see citing works
Prefrontal responses to drug cues: a neurocognitive analysis
Wilson, S. J., Sayette, M. A., & Fiez, J. A. (2004) · Nature Neuroscience · doi:10.1038/nn1200 · Cited by 408 · see citing works
Involvement of the dorsal striatum in cue-controlled cocaine seeking
Vanderschuren, L. J. M. J., Di Ciano, P., & Everitt, B. J. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0925-05.2005 · Cited by 393 · see citing works
McLaughlin, J., & See, R. E. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1196-x · Cited by 392 · see citing works
Inactivation of the Interoceptive Insula Disrupts Drug Craving and Malaise Induced by Lithium
Contreras, M., Ceric, F., & Torrealba, F. (2007) · Science · doi:10.1126/science.1145590 · Cited by 297 · see citing works
Childress, A. R., McLellan, A. T., & O’Brien, C. P. (1986) · British Journal of Addiction · doi:10.1111/j.1360-0443.1986.tb00385.x · Cited by 258 · see citing works
Neural substrates of conditioned-cued relapse to drug-seeking behavior
See, R. E. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00682-7 · Cited by 257 · see citing works
Neural substrates of cocaine-cue associations that trigger relapse
See, R. E. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.09.034 · Cited by 228 · see citing works
Procedure for minimizing stress for fMRI studies in conscious rats
King, J. A., Garelick, T. S., Brevard, M. E., Chen, W., Messenger, T. L., Duong, T. Q., & Ferris, C. F. (2005) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2005.04.011 · Cited by 228 · see citing works
Wilson, M., & Shepherd, G. M. (1998) · Cited by 224 · see citing works
Orbitomedial prefrontal cortical projections to hypothalamus in the rat
Floyd, N. S., Price, J. L., Ferry, A. T., Keay, K. A., & Bandler, R. J. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1105 · Cited by 175 · see citing works
Neuroimaging for drug addiction and related behaviors
Parvaz, M. A., Alia-Klein, N., Woicik, P. A., Volkow, N. D., & Goldstein, R. Z. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.055 · Cited by 151 · see citing works
NEVILLE, K. R., & Haberly, L. B. (2004) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195159561.003.0010 · Cited by 145 · see citing works
Bradberry, C. W., Barrett-Larimore, R. L., Jatlow, P., & Rubino, S. R. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-10-03874.2000 · Cited by 137 · see citing works
Imaging the neural circuitry and chemical control of aggressive motivation
Ferris, C. F., Stolberg, T. L., Kulkarni, P. P., Murugavel, M., Blanchard, R. J., Blanchard, D. C., Febo, M., Brevard, M. E., & Simon, N. G. (2008) · BMC Neuroscience · doi:10.1186/1471-2202-9-111 · Cited by 124 · see citing works
Self-citationThe Neural Consequences of Repeated Cocaine Exposure Revealed by Functional MRI in Awake Rats
Febo, M., Segarra, A. C., Nair, G., Schmidt, K. F., Duong, T. Q., & Ferris, C. F. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300653 · Cited by 113 · see citing works
Self-citationSelf-stimulation in the frontal cortex of rattus norvegicus
Routtenberg, A., & Sloan, M. A. (1972) · Behavioral Biology · doi:10.1016/s0091-6773(72)80218-9 · Cited by 110 · see citing works
Di Pietro, N. C., Black, Y. D., & Kantak, K. M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05193.x · Cited by 107 · see citing works
MR properties of rat sciatic nerve following trauma
Stanisz, G. J., Midha, R., Munro, C. A., & Henkelman, R. M. (2001) · Magnetic Resonance in Medicine · doi:10.1002/1522-2594(200103)45:3 · Cited by 95 · see citing works
Campbell, K. A., Evans, G. J., & Gallistel, C. R. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90315-4 · Cited by 78 · see citing works
Chen, Y. I., Mandeville, J. B., Nguyen, T. V., Talele, A. C., CAVAGNA, F. M., & Jenkins, B. G. (2001) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.1215 · Cited by 78 · see citing works
Deroche‐Gamonet, V., Piat, F., Moal, M. L., & Piazza, P. V. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01974.x · Cited by 69 · see citing works
Deconstructing Craving: Dissociable Cortical Control of Cue Reactivity in Nicotine Addiction
Scott, D., & Hiroi, N. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.01.023 · Cited by 63 · see citing works
Activation of neurones in the prefrontal cortex by brain-stimulation reward in the rat
Rolls, E. T., & Cooper, S. J. (1973) · Brain Research · doi:10.1016/0006-8993(73)90795-6 · Cited by 49 · see citing works
Encoding of reward expectation by monkey anterior insular neurons
Mizuhiki, T., Richmond, B. J., & Shidara, M. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00282.2011 · Cited by 41 · see citing works
Effects of cocaine and GBR-12909 on brain stimulation reward
Maldonado-Irizarry, C. S., Stellar, J. R., & Kelley, A. E. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90200-3 · Cited by 34 · see citing works
Self-citationBaeg, E. H., Jackson, M., Jedema, H. P., & Bradberry, C. W. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3206-09.2009 · Cited by 31 · see citing works
Dobrovitsky, V., Pimentel, P., Duarte, A., Froestl, W., Stellar, J. R., & Trzcińska, M. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00007-2 · Cited by 24 · see citing works
Self-citationLu, H., Chefer, S. I., Kurup, P. K., Guillem, K., Vaupel, D. B., Ross, T. J., Moore, A. V., Yang, Y., Peoples, L. L., & Stein, E. A. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.05.076 · Cited by 23 · see citing works
Rodríguez-Borrero, E., Bernardo‐Colón, A., BURGOSMARTIR, M., ALVAREZCARILLO, J., ESTRADADELCAMPO, Y., ABELLARAMIREZ, C., & Maldonado-Vlaar, C. S. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.07.034 · Cited by 14 · see citing works
Su, Z., Kichaev, G., Wenzel, J. M., Ben‐Shahar, O., & Ettenberg, A. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.10.006 · Cited by 6 · see citing works
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Research works printed but not linked: 1
- [36]Stellar JR Rice MB Pharmacological basis of intracranial self-stimulation Liebman JM Copper SJ The pharmacological basis of reward Clarendon Press Oxford, UK 1989 14 65
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Jonckers, E., Shah, D., Hamaide, J., Verhoye, M., & der Linden, A. V. (2015) · Frontiers in Pharmacology · doi:10.3389/fphar.2015.00231 · Cited by 120 · see citing works
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Harris, A. P., Lennen, R. J., Marshall, I., Jansen, M. A., Pernet, C. R., Brydges, N. M., Duguid, I., & Holmes, M. C. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12939 · Cited by 60 · see citing works
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Ferris, C. F. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.854377 · Cited by 45 · see citing works
Low, L. A., Bauer, L. C., Pitcher, M. H., & Bushnell, M. C. (2016) · Pain · doi:10.1097/j.pain.0000000000000579 · Cited by 43 · see citing works
Gisquet-Verrier, P., & Dorze, C. L. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00026 · Cited by 30 · see citing works
Sakurai, K., Shintani, T., Jomura, N., Matsuda, T., Sumiyoshi, A., & Hisatsune, T. (2020) · Scientific Reports · doi:10.1038/s41598-020-60894-7 · Cited by 16 · see citing works
Caffrey, M. K., & Febo, M. (2013) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2013.09.032 · Cited by 14 · see citing works
Self-citationLowen, S. B., Rohan, M. L., Gillis, T. E., Thompson, B. S., Wellons, C. B. W., & Andersen, S. L. (2015) · NeuroImage: Clinical · doi:10.1016/j.nicl.2015.06.012 · Cited by 11 · see citing works
Conceição, N. D. S., dos Santos, G. F. S., Rodrigues, J. G. A., Junior, S. D. B. G., Romão, W., & Ferreira, R. D. Q. (2024) · Microchemical Journal · doi:10.1016/j.microc.2024.110723 · Cited by 9 · see citing works
Gisquet-Verrier, P., Tolédano, D., & Dorze, C. L. (2016) · Therapies · doi:10.1016/j.therap.2016.07.005 · Cited by 8 · see citing works
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Doi, T., Iwasa, S., Muro, K., Satoh, T., Hironaka, S., Esaki, T., Nishina, T., Hara, H., Machida, N., Komatsu, Y., et al. (2018) · Annals of Oncology · doi:10.1093/annonc/mdy282.043 · Cited by 2 · see citing works
- Authors
- Johnson, T. R., Smerkers, B., Moulder, J. K., Stellar, J. R., & Febo, M.
- Affiliations
- Northeastern University (US)
- Corresponding author
- Febo, Marcelo
- ORCID
- Febo, Marcelo
- Venue
- Neuroscience Letters
- Publisher
- Elsevier BV
- Published
- 2013-02
- Volume
- 534
- Pages
- 160-165
- ISSN
- 0304-3940 (ISSN-L)
- PMC
- PMC3809094
- OpenAlex
- W2052457717
- Cited by
- 15
- References
- 42
- Citations by year
- 2024: 2 · 2023: 1 · 2022: 1 · 2021: 1 · 2020: 1 · 2019: 1 · 2018: 1 · 2016: 3 · 2015: 3 · 2013: 1
- FWCI
- 0.53
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neuroscience Letters (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Whitehall Foundation
- NIH (DA019946)
- Northeastern University
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- cocaine, olfactory conditioning, insula, reward threshold, brain stimulation, BOLD activation, drug cues
- MeSH terms
- Animals, Brain, Brain Mapping, Cocaine, Conditioning, Operant, Cues, Electric Stimulation, Magnetic Resonance Imaging, Male, Odorants, Reward, Sensory Thresholds, Wakefulness, Rats, Sprague-Dawley, Rats
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