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Thalamo-cortical spatio-temporal dynamics and its alterations in human brain pathology
NeuroImage
11, Number
5, 2000,
Part 2 of 2 Parts 1 DE
bl@
DISORDERS - NEUROLOGY
Thalamo-cortical
spatio-temporal dynamics and its alterations in human brain pathology
U. Ribary*, D. Jeanmonod?, E. Kronberg*, J. Schulman*, R. Ramirez*, P. MitraS, R. Llinais*
K. SauvC*,
*CNM, Dept. Physiology and Neuroscience, New York University School of Medicine, New York, NY, USA tDept. Neurosurgery, University Hospital of Zurich, Zurich, Switzerland $Bell Laboratories, Lucent Technologies, Murray Hill, NJ, USA Introduction Over the past years our magneto-encephalographic (MEG) studies have indicated that cognitive activity is associated with gamma band (30.50Hz) activity in the human brain (1, 2). This oscillatory activity was found to be resetable, at the level of the thalamo-cortical systems, by sensory stimulation Moreover, coherent gamma band activity has been related to the temporal binding of auditory (3) and tactile stimuli (4). This oscillatory rhythmicity appears to be the temporal binding mechanism responsible for the conjunction of the different sensory inputs into a single cognitive experience (2), demonstrating a precise timing of thalamo-cortical networks in the healthy human brain. Our MEG studies provided further evidence for a slight dysrhythmia within thalamo-cortical systems in subjects with Language-Based Learning Disabilities (5). Clearly an alteration of precise timing of thalamo-cortical networks correlated to altered behavioral patterns, namely to altered perception of sensory input. These findings let us suggest that a dysrhythmia within thalamo-cortical systems could represent a key issue underlying various pathological behavioral symptoms observed in neuropsychiatry. Methods We analyzed spontaneous brain activity from 9 healthy control subjects and from 9 patients suffering from chronic severe and therapy-resistant neurological or neuropsychiatric disorders, including 4 patients diagnosed with Parkinson’s disease, 1 patient with tin&us, 2 patients with neurogenic pain, and 2 patients with major depression. Magnetic recordings were obtained at our laboratory with a whole-head 14%channel MEG system (BTi). During the recording sessions the subject was placed on a bed with the MEG recording port surrounding the subject’s head in order to record the magnetic fields from different angles over the head surface. Spontaneous brain activity was continuously recorded for 10 mm while the subject rested with eyes closed (bandpass: 0.1.lOOHz, sample rate 508 Hz). The EKG was simultaneously recorded digitally for off-line heart-artifact rejection. Continuous MEG raw data were analyzed on a LJNUX cluster computer system, using in-house software and commercial Matlab analysis software packages (6). Results
and Discussion
Recent spontaneous MEG activity was recorded in awake healthy human controls and in patients suffering from neurogenic pain, tin&us, Parkinson’s disease or depression (6). Compared to controls, patients showed increased low frequency theta rhythmicity in conjunction with a widespread and marked increase of coherence among high and low frequency oscillations. These data indicate the presence of a thalamo-cortical dysrhythmia which we propose is responsible for all the above mentioned conditions. This coherent theta activity, the result of a resonant interaction between thalamus and cortex, is due on the generation of low threshold calcium spike bursts by thalamic cells (7). The presence of these bursts is directly related to thalamic cell hyperpolarization, brought about by either excess inhibition or disfacilitation. The emergence of positive clinical symptoms is viewed as resulting from ectopic gamma band activation, which we refer to as the “edge effect”. This effect is observable as increased coherence between low and high frequency oscillations probably resulting from inhibitory asymmetry between high and low frequency thalamo-cortical modules at the cortical level. References !. Ribary, U., iuannides, A.A., Singh, KD., Hasson. R.. Bolton. JPR.. Lado. F.. Mogilner. A.. and Llinris, R. Proc. Nat]. Acad. Sci. USA, 1991. X8:11037-1 1041. 2. Llinas, R.. and Ribary, U. Proc. Natl. Acad. Sci. USA, 1993. 90:2078-2081. 3. Joliot, M., Ribary, U., and Llinb, R. Proc. Natl. Acad. Sci. USA, 1994. 91:11748-l 1751. 3. Sauve, K.. Wang, G.. Rolli, M., Jagow, R., Kronberg, E., Ribary, U. and Llinas, R. Sot. Neurosci. Abstr., 1998, 24: 1128. 5. Llinas, R., Ribary, U. and Tallal, P. In: Basic Mechanisms in Cognition and Language, C.VonEuler, I. Lundberg and R. Llinas, eds., Elsevier Science. New York, pp. 101-108, 1998. 6. Llinas, R., Ribary, U., Jeanmonod, D., Kronberg, E. and Mitra, P. Proc. Natl. Acad. Sci. USA, 1999, 96: 15222-15227. 7. Jahnsen, H., and Llinas, R. J.Physiol. (London), 1984, 349205.226.
Support: The Charles A. Dana Foundation, NYU Medical Biomagnetic Technologies Inc., and Lucent Technologies
Center General Clinical Internal Funds.
S168
Research
Center
(NIH-NCRR
MO1 RROOO96),
11, Number
5, 2000,
Part 2 of 2 Parts 1 DE
bl@
DISORDERS - NEUROLOGY
Thalamo-cortical
spatio-temporal dynamics and its alterations in human brain pathology
U. Ribary*, D. Jeanmonod?, E. Kronberg*, J. Schulman*, R. Ramirez*, P. MitraS, R. Llinais*
K. SauvC*,
*CNM, Dept. Physiology and Neuroscience, New York University School of Medicine, New York, NY, USA tDept. Neurosurgery, University Hospital of Zurich, Zurich, Switzerland $Bell Laboratories, Lucent Technologies, Murray Hill, NJ, USA Introduction Over the past years our magneto-encephalographic (MEG) studies have indicated that cognitive activity is associated with gamma band (30.50Hz) activity in the human brain (1, 2). This oscillatory activity was found to be resetable, at the level of the thalamo-cortical systems, by sensory stimulation Moreover, coherent gamma band activity has been related to the temporal binding of auditory (3) and tactile stimuli (4). This oscillatory rhythmicity appears to be the temporal binding mechanism responsible for the conjunction of the different sensory inputs into a single cognitive experience (2), demonstrating a precise timing of thalamo-cortical networks in the healthy human brain. Our MEG studies provided further evidence for a slight dysrhythmia within thalamo-cortical systems in subjects with Language-Based Learning Disabilities (5). Clearly an alteration of precise timing of thalamo-cortical networks correlated to altered behavioral patterns, namely to altered perception of sensory input. These findings let us suggest that a dysrhythmia within thalamo-cortical systems could represent a key issue underlying various pathological behavioral symptoms observed in neuropsychiatry. Methods We analyzed spontaneous brain activity from 9 healthy control subjects and from 9 patients suffering from chronic severe and therapy-resistant neurological or neuropsychiatric disorders, including 4 patients diagnosed with Parkinson’s disease, 1 patient with tin&us, 2 patients with neurogenic pain, and 2 patients with major depression. Magnetic recordings were obtained at our laboratory with a whole-head 14%channel MEG system (BTi). During the recording sessions the subject was placed on a bed with the MEG recording port surrounding the subject’s head in order to record the magnetic fields from different angles over the head surface. Spontaneous brain activity was continuously recorded for 10 mm while the subject rested with eyes closed (bandpass: 0.1.lOOHz, sample rate 508 Hz). The EKG was simultaneously recorded digitally for off-line heart-artifact rejection. Continuous MEG raw data were analyzed on a LJNUX cluster computer system, using in-house software and commercial Matlab analysis software packages (6). Results
and Discussion
Recent spontaneous MEG activity was recorded in awake healthy human controls and in patients suffering from neurogenic pain, tin&us, Parkinson’s disease or depression (6). Compared to controls, patients showed increased low frequency theta rhythmicity in conjunction with a widespread and marked increase of coherence among high and low frequency oscillations. These data indicate the presence of a thalamo-cortical dysrhythmia which we propose is responsible for all the above mentioned conditions. This coherent theta activity, the result of a resonant interaction between thalamus and cortex, is due on the generation of low threshold calcium spike bursts by thalamic cells (7). The presence of these bursts is directly related to thalamic cell hyperpolarization, brought about by either excess inhibition or disfacilitation. The emergence of positive clinical symptoms is viewed as resulting from ectopic gamma band activation, which we refer to as the “edge effect”. This effect is observable as increased coherence between low and high frequency oscillations probably resulting from inhibitory asymmetry between high and low frequency thalamo-cortical modules at the cortical level. References !. Ribary, U., iuannides, A.A., Singh, KD., Hasson. R.. Bolton. JPR.. Lado. F.. Mogilner. A.. and Llinris, R. Proc. Nat]. Acad. Sci. USA, 1991. X8:11037-1 1041. 2. Llinas, R.. and Ribary, U. Proc. Natl. Acad. Sci. USA, 1993. 90:2078-2081. 3. Joliot, M., Ribary, U., and Llinb, R. Proc. Natl. Acad. Sci. USA, 1994. 91:11748-l 1751. 3. Sauve, K.. Wang, G.. Rolli, M., Jagow, R., Kronberg, E., Ribary, U. and Llinas, R. Sot. Neurosci. Abstr., 1998, 24: 1128. 5. Llinas, R., Ribary, U. and Tallal, P. In: Basic Mechanisms in Cognition and Language, C.VonEuler, I. Lundberg and R. Llinas, eds., Elsevier Science. New York, pp. 101-108, 1998. 6. Llinas, R., Ribary, U., Jeanmonod, D., Kronberg, E. and Mitra, P. Proc. Natl. Acad. Sci. USA, 1999, 96: 15222-15227. 7. Jahnsen, H., and Llinas, R. J.Physiol. (London), 1984, 349205.226.
Support: The Charles A. Dana Foundation, NYU Medical Biomagnetic Technologies Inc., and Lucent Technologies
Center General Clinical Internal Funds.
S168
Research
Center
(NIH-NCRR
MO1 RROOO96),