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Neuroanatomical correlates of brainstem coma
Abstract
The brainstem tegmentum, including the reticular formation, contains distinct nuclei, each of which has a set of chemical, physiological and anatomical features. Damage to the brainstem tegmentum is known to cause coma, the most radical disturbance of consciousness. However, it has remained unclear which nuclei within the tegmentum are crucial for the maintenance of consciousness in humans. Accordingly, we initiated a retrospective study of MRIs obtained from 47 patients with brainstem stroke. The lesion boundaries were charted on patient MRIs and transferred onto a corresponding series of 4.7 T MRIs obtained from a control brainstem specimen that later was cut on a freezing microtome and analysed histologically. In addition, medical charts and available post-mortem materials were used to obtain relevant clinical and anatomical data to verify the MRI readings in each case. We found that in the 38 patients who did not have coma, brainstem damage either was located outside the tegmentum (n = 29) or produced a very small and unilateral compromise of the tegmentum (n = 9). In contrast, in patients who had coma (n = 9), the lesions in the tegmentum were mostly bilateral (n = 7) and were located either in the pons alone (n = 4) or in the upper pons and the midbrain (n = 5). The maximum overlap territory of the lesions coincided with the location of the rostral raphe complex, locus coeruleus, laterodorsal tegmental nucleus, nucleus pontis oralis, parabrachial nucleus and the white matter in between these nuclei. We also found that four coma subjects developed hyperthermia and died in the absence of any infections. In these cases, the maximum lesion overlap was centred in the core of pontine tegmentum. Our findings suggest that lesions confined to the upper pons can cause coma in humans even in the absence of damage to the midbrain. The findings also point to the brainstem nuclei whose lesions are likely to be associated with loss of consciousness and fatal hyperthermia in humans.
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“Similarly, in patients with brainstem stroke, Parvizi and Damasio found that acute coma was associated with magnetic resonance imaging (MRI) lesions in the pontine tegmentum extending from the upper pons into the midbrain.7”
From Damage to Arousal-Promoting Brainstem Neurons with Traumatic Brain Injury (2016) · cites this paper as [7]
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“Still, it remains unknown whether TBI injures these specific arousalpromoting neurons.”
From Damage to Arousal-Promoting Brainstem Neurons with Traumatic Brain Injury (2016) · cites this paper as [7]
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“Each of the five sites selected by LDA may influence consciousness: the pons and posterior fossa, where the reticular activating system is located; the thalamus, whose reticular and intralaminar nuclei belong to the consciousness pathway (33); the lenticular nuclei, which is near the hypothalamus and basal forebrain;…”
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Long-Term White Matter Changes after Severe Traumatic Brain Injury: A 5-Year Prospective Cohort
Dinkel, J., Drier, A., Khalilzadeh, O., Perlbarg, V., Czernecki, V., Gupta, R., Gomas, F., Sanchez-Peña, P., Dormont, D., Damien Galanaud, E., et al. (2013) · American Journal of Neuroradiology · doi:10.3174/ajnr.a3616 · Cited by 69
“Available evidence indicates that damage to critical areas such as the corpus callosum or brain stem correlate most highly with poor post-TBI prognosis.(26,28,30) In a large multicenter study, we recently generated and validated a stringent prognostic model by integrating a composite DTI score of white matter tracts w…”
MethodNeurobiology of waking and sleeping
Jones, B. E. (2010) · Handbook of clinical neurology · doi:10.1016/b978-0-444-52006-7.00009-5 · Cited by 67
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript following large brainstem lesions (Plum and Posner, 1980; Parvizi and Damasio, 2003).”
BackgroundTraumatic Brain Injury and Incidence Risk of Sleep Disorders in Nearly 200,000 US Veterans
Leng, Y., Byers, A. L., Barnes, D. E., Peltz, C. B., Li, Y., & Yaffe, K. S. (2021) · Neurology · doi:10.1212/wnl.0000000000011656 · Cited by 65
What is “the unconscious,” and where is it located in the brain? A neuropsychoanalytic perspective
Solms, M. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13437 · Cited by 68
Feelings Are the Source of Consciousness
Damasio, A., & Damasio, H. (2023) · Neural Computation · doi:10.1162/neco_a_01521 · Cited by 60
Emerging from an unresponsive wakefulness syndrome: Brain plasticity has to cross a threshold level
Bagnato, S., Boccagni, C., Santangelo, A., Fingelkurts, A. A., Fingelkurts, A. A., & Galardi, G. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.09.007 · Cited by 65
“In some pathological conditions, awareness is not achievable without arousal, as has been evidenced in comatose patients with brainstem lesions but an anatomically intact cerebral cortex (Parvizi and Damasio, 2003; Laureys, 2005).”
BackgroundIs there a brainstem substrate for action selection?
Humphries, M. D., GURNEY, K. N., & Prescott, T. J. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2057 · Cited by 62
“An intact mRF is trivially necessary for action selection in the sense that lesions to specific parts of it cause coma and even death in humans (Parvizi & Damasio 2003).”
BackgroundChallenge-driven attention: Interacting frontal and brainstem systems
Raizada, R. D. S. (2008) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.003.2007 · Cited by 64
“stem can be found in Parvizi and Damasio (2003): nuclei located nearby”
BackgroundEdlow, B. L., Giacino, J. T., Hirschberg, R. E., Gerrard, J. L., Wu, O., & Hochberg, L. R. (2013) · Neurocritical Care · doi:10.1007/s12028-013-9870-x · Cited by 61
“Recovery of arousal has been described in MRI studies of patients with unilateral brainstem TAI [7] and patients with unilateral ischemic lesions in the brainstem [49].”
BackgroundDupre, C. M., Libman, R., Dupre, S. I., Katz, J. M., Rybinnik, I., & Kwiatkowski, T. (2013) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2013.07.015 · Cited by 61
Direct Parabrachial–Cortical Connectivity
Grady, F. S., Peltekian, L., Iverson, G. N., & Geerling, J. C. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa072 · Cited by 61
van der Eerden, A. W., Khalilzadeh, O., Perlbarg, V., Dinkel, J., Sanchez-Peña, P., Vos, P. E., Luyt, C. E., Stevens, R. D., de Champfleur, N. M., Delmaire, C., et al. (2013) · Radiology · doi:10.1148/radiol.13122720 · Cited by 60
Gao, S., Proekt, A., Renier, N., Calderon, D. P., & Pfaff, D. W. (2019) · Nature Communications · doi:10.1038/s41467-019-10797-7 · Cited by 56
Boes, A. D., Fischer, D. B., Geerling, J. C., Bruss, J., Saper, C. B., & Fox, M. (2018) · SLEEP · doi:10.1093/sleep/zsy108 · Cited by 53
Medial Parabrachial Nucleus Is Essential in Controlling Wakefulness in Rats
Xu, Q., Wang, D.-R., Dong, H., Chen, L., Lu, J., Lazarus, M., Chérasse, Y., Chen, G.-H., Qu, W., & Huang, Z. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.645877 · Cited by 52
Why acute unilateral vestibular cortex lesions mostly manifest without vertigo
Dieterich, M., & Brandt, T. (2015) · Neurology · doi:10.1212/wnl.0000000000001501 · Cited by 50
Synthetic consciousness: the distributed adaptive control perspective
Verschure, P. F. M. J. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0448 · Cited by 54
Damage to Arousal-Promoting Brainstem Neurons with Traumatic Brain Injury
Valko, P. O., Gavrilov, Y. V., Yamamoto, M., Noaín, D., Reddy, H., Haybaeck, J., Weis, S., Baumann, C. R., & Scammell, T. E. (2016) · Sleep · doi:10.5665/sleep.5844 · Cited by 49
Neural correlates of consciousness: what we know and what we have to learn!
Calabrò, R. S., Cacciola, A., Bramanti, P., & Milardi, D. (2015) · Neurological Sciences · doi:10.1007/s10072-015-2072-x · Cited by 49
Thalamic strokes that severely impair arousal extend into the brainstem
Hindman, J., Bowren, M. D., Bruss, J., Wright, B., Geerling, J. C., & Boes, A. D. (2018) · Annals of Neurology · doi:10.1002/ana.25377 · Cited by 49
Kinkingnéhun, S., Emmanuelle Volle, C., Pélégrini‐Issac, M., Golmard, J., Lehéricy, S., Boisguéheneuc, F. D., Zhang-Nunes, S., Sosson, D., Duffau, H., Samson, Y., et al. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.06.027 · Cited by 48
Advanced Neuroimaging in Traumatic Brain Injury
Wu, O., & Edlow, B. L. (2013) · Seminars in Neurology · doi:10.1055/s-0032-1331810 · Cited by 50
Abulafia, R., Zalkind, V. I., & Devor, M. G. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1357-08.2009 · Cited by 47
“It should be noted, however, that imaging in humans routinely reveals altered activity in an upper mesopontine region consistent with the MPTA (Paus, 2000; Parvizi and Damasio, 2003).”
BackgroundDamásio, A. R., & Meyer, K. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-374168-4.00001-0 · Cited by 45
Weiss, N., Damien Galanaud, E., Carpentier, A. C., du Montcel, S. T., Naccache, L., Coriat, P., & Puybasset, L. (2008) · Journal of Neurology · doi:10.1007/s00415-008-0658-4 · Cited by 46
“Parvizi and Damasio [22] also observed that patients who were in coma after a brainstem stroke had mostly bilateral lesions of the tegmentum.”
BackgroundMechanisms of Neurologic Failure in Critical Illness
Pustavoitau, A., & Stevens, R. D. (2008) · Critical Care Clinics · doi:10.1016/j.ccc.2007.11.004 · Cited by 45
“To result in coma, lesions must involve both hemispheres or must be unilateral lesions large enough to displace midline structures significantly (compartmental shift); diencephalic and brainstem injury resulting in coma may be relatively small, but coma typically is seen only with midline or bilateral involvement [39].”
BackgroundStiver, S. I., Gean, A. D., & Manley, G. T. (2008) · Journal of neurosurgery · doi:10.3171/2008.8.jns08314 · Cited by 43
Homeostatic feelings and the biology of consciousness
Damasio, A., & Damasio, H. (2022) · Brain · doi:10.1093/brain/awac194 · Cited by 42
Raguž, M., Predrijevac, N., Dlaka, D., Orešković, D., Rotim, A., Romić, D., Almahariq, F., Marčinković, P., Deletis, V., Kostović, I., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-83873-y · Cited by 43
Alnagger, N., Cardone, P., Martial, C., Laureys, S., Annen, J., & Gosseries, O. (2023) · Presse medicale · doi:10.1016/j.lpm.2022.104163 · Cited by 31
Functional MRI and Outcome in Traumatic Coma
Edlow, B. L., Giacino, J. T., & Wu, O. (2013) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-013-0375-y · Cited by 41
“This goal is fundamentally important to predicting recovery after traumatic coma, because the human ARAS network appears to contain redundant circuitry that may make possible recovery of arousal when some, but not all components of the network are disrupted [98].”
Functional neuroimaging of primary headache disorders
Cohen, A. S., & Goadsby, P. J. (2006) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.6.8.1159 · Cited by 39
Current Concepts in the Pharmacotherapy of Pseudobulbar Affect
Pioro, E. P. (2011) · Drugs · doi:10.2165/11591450-000000000-00000 · Cited by 38
“sions are best known for their association with coma.([54]) In support of SSRIs, it has also been noted([25]) that the facial-nerve nuclei are rich in serotonin receptors.”
Background
Metadata
- Authors
- Parvizi, J.
- Affiliations
- University of Iowa (US)
- Corresponding author
- Parvizi, J.
- ORCID
- Parvizi, J.
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2003-04-22
- Volume
- 126
- Issue
- 7
- Pages
- 1524-1536
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- OpenAlex
- W2045226019
- Cited by
- 400
- References
- 74
- Citations by year
- 2026: 17 · 2025: 27 · 2024: 27 · 2023: 23 · 2022: 16 · 2021: 19 · 2020: 18 · 2019: 20 · 2018: 36 · 2017: 13 · 2016: 20 · 2015: 14 · 2014: 14 · 2013: 30 · 2012: 15
- FWCI
- 3.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain (publishedVersion)
- PubMed (publishedVersion)
- Funders
- G. Harold and Leila Y. Mathers Foundation
- University of Illinois at Urbana-Champaign
- Topics
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Keywords
- brainstem infarction, reticular formation, consciousness, pontine tegmentum, locus coeruleus, laterodorsal tegmental nucleus, parabrachial nucleus, hyperthermia, lesion localization, midbrain
- MeSH terms
- Adult, Aged, Brain Stem, Coma, Female, Fever, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Pons, Reticular Formation, Retrospective Studies, Stroke
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