E.L., a modern-day Phineas Gage: Revisiting frontal lobe injury
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Tipo de produção
article
Data de publicação
2022
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Autores
FREITAS, Pedro H. M. de
MONTEIRO, Ruy C.
BERTANI, Raphael
PERRET, Caio M.
RODRIGUES, Pedro C.
VICENTINI, Joana
MORAIS, Tagore M. Gonzalez de
ROZENTAL, Stefano F. A.
GALVAO, Gustavo F.
MATTOS, Fabricio de
Citação
LANCET REGIONAL HEALTH-AMERICAS, v.14, article ID 100340, 17p, 2022
Resumo
Background How the prefrontal cortex (PFC) recovers its functionality following lesions remains a conundrum. Recent work has uncovered the importance of transient low-frequency oscillatory activity (LFO; < 4 Hz) for the recovery of an injured brain. We aimed to determine whether persistent cortical oscillatory dynamics contribute to brain capability to support 'normal life' following injury. Methods In this 9-year prospective longitudinal study (08/2012-2021), we collected data from the patient E.L., a modern-day Phineas Gage, who suffered from lesions, impacting 11% of his total brain mass, to his right PFC and supplementary motor area after his skull was transfixed by an iron rod. A systematic evaluation of clinical, electrophysiologic, brain imaging, neuropsychological and behavioural testing were used to clarify the clinical significance of relationship between LFO discharge and executive dysfunctions and compare E.L.'s disorders to that attributed to Gage (1848), a landmark in the history of neurology and neuroscience. Findings Selective recruitment of the non-injured left hemisphere during execution of unimanual right-hand movements resulted in the emergence of robust LFO, an EEG-detected marker for disconnection of brain areas, in the damaged right hemisphere. In contrast, recruitment of the damaged right hemisphere during contralateral hand movement, resulted in the co-activation of the left hemisphere and decreased right hemisphere LFO to levels of controls enabling performance, suggesting a target for neuromodulation. Similarly, transcranial magnetic stimulation (TMS), used to create a temporary virtual-lesion over E.L.'s healthy hemisphere, disrupted the modulation of contralateral LFO, disturbing behaviour and impairing executive function tasks. In contrast to Gage, reasoning, planning, working memory, social, sexual and family behaviours eluded clinical inspection by decreasing LFO in the delta frequency range during motor and executive functioning. Interpretation Our study suggests that modulation of LFO dynamics is an important mechanism by which PFC accommodates neurological injuries, supporting the reports of Gages recovery, and represents an attractive target for therapeutic interventions.
Palavras-chave
Traumatic brain injury (TBI), Phineas Gage, Prefrontal cortex (PFC), Corpus callosum (C.C.), Magnetic Resonance Imaging (MRI), Neuropsychological tests, Transcranial Magnetic Stimulation, Low Frequency Oscillations
Referências
- Arciniega H, 2021, SCI REP-UK, V11, DOI 10.1038/s41598-021-80995-1
- Berlucchi G, 2012, CORTEX, V48, P36, DOI 10.1016/j.cortex.2011.04.008
- Blatow M, 2011, J MAGN RESON IMAGING, V34, P429, DOI 10.1002/jmri.22629
- Chen YH, 2016, BRIT J PSYCHIAT, V208, P160, DOI 10.1192/bjp.bp.114.156075
- Cohen JD, 1997, NATURE, V386, P604, DOI 10.1038/386604a0
- Colom R, 2003, PERS INDIV DIFFER, V34, P33, DOI 10.1016/S0191-8869(02)00023-5
- Crowley K, 2005, SLEEP, V28, P865, DOI 10.1093/sleep/28.7.865
- Dang-Vu TT, 2008, P NATL ACAD SCI USA, V105, P15160, DOI 10.1073/pnas.0801819105
- Gazzaniga MS, 2009, NEUROLOGY OF CONSCIOUSNESS: COGNITIVE NEUROSCIENCE AND NEUROPATHOLOGY, P261, DOI 10.1016/B978-0-12-374168-4.00020-4
- Gazzaniga MS, 2000, BRAIN, V123, P1293, DOI 10.1093/brain/123.7.1293
- GLOOR P, 1977, NEUROLOGY, V27, P326, DOI 10.1212/WNL.27.4.326
- Goldberg E, 2005, PSYCHIAT CLIN N AM, V28, P567, DOI 10.1016/j.psc.2005.05.005
- Harlow John M., 1993, Publications of the Massachusetts Medical Society, V4, P274, DOI 10.1177/0957154X9300401407
- Harmony T, 2013, FRONT INTEGR NEUROSC, V7, DOI 10.3389/fnint.2013.00083
- Huang MX, 2012, NEUROIMAGE, V61, P1067, DOI 10.1016/j.neuroimage.2012.04.029
- Huber R, 2004, NATURE, V430, P78, DOI 10.1038/nature02663
- Husain M, 2003, NAT REV NEUROSCI, V4, P26, DOI 10.1038/nrn1005
- Kessels R P, 2000, Appl Neuropsychol, V7, P252, DOI 10.1207/S15324826AN0704_8
- Kinnunen KM, 2011, BRAIN, V134, P449, DOI 10.1093/brain/awq347
- Lee MY, 2013, NEUROSCI LETT, V533, P7, DOI 10.1016/j.neulet.2012.11.041
- Llinás RR, 2006, J NEUROPHYSIOL, V95, P3297, DOI 10.1152/jn.00166.2006
- Lundstrom BN, 2019, SCI REP-UK, V9, DOI 10.1038/s41598-019-42347-y
- Luria A. R., 1966, Higher cortical functions in man
- Massimini M, 2005, SCIENCE, V309, P2228, DOI 10.1126/science.1117256
- Massimini M, 2007, P NATL ACAD SCI USA, V104, P8496, DOI 10.1073/pnas.0702495104
- McIntosh RD, 2021, CORTEX, V135, P146, DOI 10.1016/j.cortex.2020.11.005
- Mecarelli O, 2004, ANN PHARMACOTHER, V38, P1816, DOI 10.1345/aph.1E136
- Munoz DP, 2004, NAT REV NEUROSCI, V5, P218, DOI 10.1038/nrn1345
- Mutha PK, 2012, J MOTOR BEHAV, V44, P455, DOI 10.1080/00222895.2012.747482
- Nair DG, 2007, NEUROIMAGE, V34, P253, DOI 10.1016/j.neuroimage.2006.09.010
- Nardone R, 2020, BRAIN RES BULL, V159, P44, DOI 10.1016/j.brainresbull.2020.03.016
- Narikiyo K, 2020, NAT NEUROSCI, V23, P741, DOI 10.1038/s41593-020-0625-7
- O'Reilly JX, 2013, P NATL ACAD SCI USA, V110, P13982, DOI 10.1073/pnas.1305062110
- Parker RI, 2009, BEHAV THER, V40, P357, DOI 10.1016/j.beth.2008.10.006
- Perez MA, 2014, J NEUROPHYSIOL, V111, P405, DOI 10.1152/jn.00322.2013
- Sacks O, 2008, ANN NEUROL, V63, P129, DOI 10.1002/ana.21378
- Salat DH, 1999, ARCH NEUROL-CHICAGO, V56, P338, DOI 10.1001/archneur.56.3.338
- Savazzi S, 2007, NEUROPSYCHOLOGIA, V45, P2417, DOI 10.1016/j.neuropsychologia.2007.04.002
- Schmidt MF, 2003, J NEUROPHYSIOL, V90, P3931, DOI 10.1152/jn.00003.2003
- Schwalm M, 2017, ELIFE, V6, DOI 10.7554/eLife.27602
- SLICK D, 2006, COMPENDIUM NEUROPSYC, P1
- STERIADE M, 1993, J NEUROSCI, V13, P3266
- Theyel BB, 2010, NAT NEUROSCI, V13, P84, DOI 10.1038/nn.2449
- Tombu M, 2003, J EXP PSYCHOL HUMAN, V29, P3, DOI 10.1037/0096-1523.29.1.3
- Tyszka JM, 2011, J NEUROSCI, V31, P15154, DOI 10.1523/JNEUROSCI.1453-11.2011
- Uddin LQ, 2008, NEUROREPORT, V19, P703, DOI 10.1097/WNR.0b013e3282fb8203
- van Horn JD, 2012, PLOS ONE, V7, DOI 10.1371/journal.pone.0037454
- Vesuna S, 2020, NATURE, V586, P87, DOI 10.1038/s41586-020-2731-9
- Walsh V, 2000, NAT REV NEUROSCI, V1, P73, DOI 10.1038/35036239
- Weiller C, 1996, NEUROIMAGE, V4, P105, DOI 10.1006/nimg.1996.0034
- Yeh N, 2019, FRONT PSYCHOL, V10, DOI 10.3389/fpsyg.2019.00993
- Zhao W, 2018, NEUROIMAGE-CLIN, V20, P594, DOI 10.1016/j.nicl.2018.08.027