[en] Although disorders of consciousness (DOCs) demonstrate widely varying clinical presentations and patterns of structural injury, global down-regulation and bilateral reductions in metabolism of the thalamus and frontoparietal network are consistent findings. We test the hypothesis that global reductions of background synaptic activity in DOCs will associate with changes in the pattern of metabolic activity in the central thalamus and globus pallidus. We compared 32 [18F]fluorodeoxyglucose PETs obtained from severely brain-injured patients (BIs) and 10 normal volunteers (NVs). We defined components of the anterior forebrain mesocircuit on high-resolution T1-MRI (ventral, associative, and sensorimotor striatum; globus pallidus; central thalamus and noncentral thalamus). Metabolic profiles for BI and NV demonstrated distinct changes in the pattern of uptake: ventral and association striatum (but not sensorimotor) were significantly reduced relative to global mean uptake after BI; a relative increase in globus pallidus metabolism was evident in BI subjects who also showed a relative reduction of metabolism in the central thalamus. The reversal of globus pallidus and central thalamus profiles across BIs and NVs supports the mesocircuit hypothesis that broad functional (or anatomic) deafferentation may combine to reduce central thalamus activity and release globus pallidus activity in DOCs. In addition, BI subjects showed broad frontoparietal metabolic down-regulation consistent with prior studies supporting the link between central thalamic/pallidal metabolism and down-regulation of the frontoparietal network. Recovery of left hemisphere frontoparietal metabolic activity was further associated with command following.
Research center :
GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Disciplines :
Neurology
Author, co-author :
Fridman, Esteban A
Beattie, Bradley J
Broft, Allegra
Laureys, Steven ; Université de Liège - ULiège > Centre de recherches du cyclotron
Schiff, Nicholas D
Language :
English
Title :
Regional cerebral metabolic patterns demonstrate the role of anterior forebrain mesocircuit dysfunction in the severely injured brain
Publication date :
April 2014
Main work title :
Proceedings of the National Academy of Sciences of the United States of America
Nakase-Richardson, R., Longitudinal outcome of patients with disordered consciousness in the NIDRR TBI Model Systems Programs (2012) J Neurotrauma, 29 (1), pp. 59-65
Luauté, J., Long-term outcomes of chronic minimally conscious and vegetative states (2010) Neurology, 75 (3), pp. 246-252
Levy, D.E., Differences in cerebral blood flow and glucose utilization in vegetative versus locked-in patients (1987) Ann Neurol, 22 (6), pp. 673-682
Laureys, S., Lemaire, C., Maquet, P., Phillips, C., Franck, G., Cerebral metabolism during vegetative state and after recovery to consciousness (1999) J Neurol Neurosurg Psychiatry, 67 (1), p. 121
Schiff, N.D., Residual cerebral activity and behavioural fragments can remain in the persistently vegetative brain (2002) Brain, 125 (PART 6), pp. 1210-1234
Laureys, S., Owen, A.M., Schiff, N.D., Brain function in coma, vegetative state, and related disorders (2004) Lancet Neurol, 3 (9), pp. 537-546
Schiff, N.D., Modeling the minimally conscious state: Measurements of brain function and therapeutic possibilities (2005) Prog Brain Res, 150, pp. 473-493
Laureys, S., Schiff, N.D., Coma and consciousness: Paradigms (re)framed by neuroimaging (2012) Neuroimage, 61 (2), pp. 478-491
Gusnard, D.A., Raichle, M.E., Raichle, M.E., Searching for a baseline: Functional imaging and the resting human brain (2001) Nat Rev Neurosci, 2 (10), pp. 685-694
Eidelberg, D., Metabolic correlates of pallidal neuronal activity in Parkinson's disease (1997) Brain, 120 (PART 8), pp. 1315-1324
Fernández-Espejo, D., A role for the default mode network in the bases of disorders of consciousness (2012) Ann Neurol, 72 (3), pp. 335-343
Laureys, S., Impaired effective cortical connectivity in vegetative state: Preliminary investigation using PET (1999) Neuroimage, 9 (4), pp. 377-382
Schiff, N.D., Behavioural improvements with thalamic stimulation after severe traumatic brain injury (2007) Nature, 448 (7153), pp. 600-603
Schiff, N.D., Recovery of consciousness after brain injury: A mesocircuit hypothesis (2010) Trends Neurosci, 33 (1), pp. 1-9
Schiff, N.D., Posterior medial corticothalamic connectivity and consciousness (2012) Ann Neurol, 72 (3), pp. 305-306
Bruno, M.-A., Vanhaudenhuyse, A., Thibaut, A., Moonen, G., Laureys, S., From unresponsive wakefulness to minimally conscious PLUS and functional locked-in syndromes: Recent advances in our understanding of disorders of consciousness (2011) J Neurol, 258 (7), pp. 1373-1384
Grillner, S., Hellgren, J., Ménard, A., Saitoh, K., Wikström, M.A., Mechanisms for selection of basic motor programs-Roles for the striatum and pallidum (2005) Trends Neurosci, 28 (7), pp. 364-370
Hornykiewicz, O., Dopamine (3-hydroxytyramine) and brain function (1966) Pharmacol Rev, 18 (2), pp. 925-964
Sano, I., Distribution of catechol compounds in human brain (1959) Biochim Biophys Acta, 32, pp. 586-587
Rieck, R.W., Ansari, M.S., Whetsell Jr., W.O., Deutch, A.Y., Kessler, R.M., Distribution of dopamine D2-like receptors in the human thalamus: Autoradiographic and PET studies (2004) Neuropsychopharmacology, 29 (2), pp. 362-372
Sánchez-González, M.A., García-Cabezas, M.A., Rico, B., Cavada, C., The primate thalamus is a key target for brain dopamine (2005) J Neurosci, 25 (26), pp. 6076-6083
Freeman, A., Nigrostriatal collaterals to thalamus degenerate in parkinsonian animal models (2001) Ann Neurol, 50 (3), pp. 321-329
Volkow, N.D., Activation of orbital and medial prefrontal cortex by methylphenidate in cocaine-addicted subjects but not in controls: Relevance to addiction (2005) J Neurosci, 25 (15), pp. 3932-3939
Laureys, S., Restoration of thalamocortical connectivity after recovery from persistent vegetative state (2000) Lancet, 355 (9217), pp. 1790-1791
García-Panach, J., A voxel-based analysis of FDG-PET in traumatic brain injury: Regional metabolism and relationship between the thalamus and cortical areas (2011) J Neurotrauma, 28 (9), pp. 1707-1717
Wallis, J.D., Orbitofrontal cortex and its contribution to decision-making (2007) Annu Rev Neurosci, 30, pp. 31-56
Young, L., Damage to ventromedial prefrontal cortex impairs judgment of harmful intent (2010) Neuron, 65 (6), pp. 845-851
Sakai, K., Task set and prefrontal cortex (2008) Annu Rev Neurosci, 31, pp. 219-245
Smith, Y., Raju, D.V., Pare, J.F., Sidibe, M., The thalamostriatal system: A highly specific network of the basal ganglia circuitry (2004) Trends Neurosci, 27 (9), pp. 520-527
Galvan, A., Smith, Y., The primate thalamostriatal systems: Anatomical organization, functional roles and possible involvement in Parkinson's disease (2011) Basal Ganglia, 1 (4), pp. 179-189
Buckwalter, J.A., Parvizi, J., Morecraft, R.J., Van Hoesen, G.W., Thalamic projections to the posteromedial cortex in the macaque (2008) J Comp Neurol, 507 (5), pp. 1709-1733
Xie, G., Critical involvement of the thalamus and precuneus during restoration of consciousness with physostigmine in humans during propofol anaesthesia: A positron emission tomography study (2011) Br J Anaesth, 106 (4), pp. 548-557
Raichle, M.E., A default mode of brain function (2001) Proc Natl Acad Sci USA, 98 (2), pp. 676-682
Brown, E.N., Lydic, R., Schiff, N.D., General anesthesia, sleep, and coma (2010) N Engl J Med, 363 (27), pp. 2638-2650
Balkin, T.J., The process of awakening: A PET study of regional brain activity patterns mediating the re-establishment of alertness and consciousness (2002) Brain, 125 (PART 10), pp. 2308-2319
Demertzi, A., Soddu, A., Laureys, S., Consciousness supporting networks (2013) Curr Opin Neurobiol, 23 (2), pp. 239-244
Schiff, N.D., Moving toward a generalizable application of central thalamic deep brain stimulation for support of forebrain arousal regulation in the severely injured brain (2012) Ann N y Acad Sci, 1265, pp. 56-68
Fridman, E.A., Fast awakening from minimally conscious state with apomorphine (2009) Brain Inj, 23 (2), pp. 172-177
Gerfen, C.R., Surmeier, D.J., Modulation of striatal projection systems by dopamine (2011) Annu Rev Neurosci, 34, pp. 441-466
Mabrouk, O.S., Li, Q., Song, P., Kennedy, R.T., Microdialysis and mass spectrometric monitoring of dopamine and enkephalins in the globus pallidus reveal reciprocal interactions that regulate movement (2011) J Neurochem, 118 (1), pp. 24-33
Brefel-Courbon, C., Clinical and imaging evidence of zolpidem effect in hypoxic encephalopathy (2007) Ann Neurol, 62 (1), pp. 102-105
Victor, J.D., Drover, J.D., Conte, M.M., Schiff, N.D., Mean-field modeling of thalamocortical dynamics and a model-driven approach to EEG analysis (2011) Proc Natl Acad Sci USA, 108 (SUPPL. 3), pp. 15631-15638
Schiff, N.D., Central thalamic contributions to arousal regulation and neurological disorders of consciousness (2008) Ann N y Acad Sci, 1129, pp. 105-118
Staunton, H., Arousal by stimulation of deep-brain nuclei (2008) Nature, 452 (7183), pp. E1. , discussion E1-E2
Moll, C.K.E., Waking up the brain: A case study of stimulation-induced wakeful unawareness during anaesthesia (2009) Prog Brain Res, 177, pp. 125-145
Hassler, R., Ore, G.D., Bricolo, A., Dieckmann, G., Dolce, G., EEG and clinical arousal induced by bilateral long-term stimulation of pallidal systems in traumatic vigil coma (1969) Electroencephalogr Clin Neurophysiol, 27 (7), pp. 689-690
Herholz, K., Discrimination between Alzheimer dementia and controls by automated analysis of multicenter FDG PET (2002) Neuroimage, 17 (1), pp. 302-316
Vogt, B.A., Vogt, L., Laureys, S., Cytology and functionally correlated circuits of human posterior cingulate areas (2006) Neuroimage, 29 (2), pp. 452-466
Giacino, J.T., Kalmar, K., Whyte, J., The JFK Coma Recovery Scale-Revised: Measurement characteristics and diagnostic utility (2004) Arch Phys Med Rehabil, 85 (12), pp. 2020-2029
Laureys, S., Auditory processing in the vegetative state (2000) Brain, 123 (PART 8), pp. 1589-1601
Fox, A.S., Central amygdala nucleus (Ce) gene expression linked to increased trait-like Ce metabolism and anxious temperament in young primates (2012) Proc Natl Acad Sci USA, 109 (44), pp. 18108-18113
Eidelberg, D., Metabolic brain networks in neurodegenerative disorders: A functional imaging approach (2009) Trends Neurosci, 32 (10), pp. 548-557
Broft, A., Striatal dopamine in bulimia nervosa: A PET imaging study (2012) Int J Eat Disord, 45 (5), pp. 648-656
Tzourio-Mazoyer, N., Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain (2002) Neuroimage, 15 (1), pp. 273-289
