Neuronal correlates of functional magnetic resonance imaging in human temporal cortex

The relationship between changes in functional magnetic resonance imaging and neuronal activity remains controversial. Data collected during awake neurosurgical procedures for the treatment of epilepsy provided a rare opportunity to examine this relationship in human temporal association cortex. We obtained functional magnetic resonance imaging blood oxygen dependent signals, single neuronal activity and local field potentials from 8 to 300 Hz at 13 temporal cortical sites, from nine subjects, during paired associate learning and control measures. The relation between the functional magnetic resonance imaging signal and the electrophysiologic parameters was assessed in two ways: colocalization between significant changes in these signals on the same paired associate-control comparisons and multiple linear regressions of the electrophysiologic measures on the functional magnetic resonance imaging signal, across all tasks. Significant colocalization was present between increased functional magnetic resonance imaging signals and increased local field potentials power in the 50–250 Hz range. Local field potentials power greater than 100 Hz was also a significant regressor for the functional magnetic resonance imaging signal, establishing this local field potentials frequency range as a neuronal correlate of the functional magnetic resonance imaging signal. There was a trend for a relation between power in some low frequency local field potentials frequencies and the functional magnetic resonance imaging signal, for 8–15 Hz increases in the colocalization analysis and 16–23 Hz in the multiple linear regression analysis. Neither analysis provided evidence for an independent relation to frequency of single neuron activity.

[1]  Werner Lutzenberger,et al.  Dynamics of Gamma-Band Activity during an Audiospatial Working Memory Task in Humans , 2002, The Journal of Neuroscience.

[2]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

[3]  Ehren L. Newman,et al.  Learning your way around town: How virtual taxicab drivers learn to use both layout and landmark information , 2007, Cognition.

[4]  Arne D. Ekstrom,et al.  Human hippocampal theta activity during virtual navigation , 2005, Hippocampus.

[5]  S. Engel,et al.  Dynamics of the Hippocampus During Encoding and Retrieval of Face-Name Pairs , 2003, Science.

[6]  R. Woods,et al.  Mathematical/computational challenges in creating deformable and probabilistic atlases of the human brain , 2000, Human brain mapping.

[7]  Koiti Motokawa.  Über den Mechanismus der Entstehung und Hemmung der α=Wellen des Hirnpotentials , 1943 .

[8]  Arne D. Ekstrom,et al.  Cellular networks underlying human spatial navigation , 2003, Nature.

[9]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

[10]  T. Rasmussen,et al.  INTRACAROTID INJECTION OF SODIUM AMYTAL FOR THE LATERALIZATION OF CEREBRAL SPEECH DOMINANCE EXPERIMENTAL AND CLINICAL OBSERVATIONS , 1960 .

[11]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[12]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[13]  Ehren L. Newman,et al.  Human θ Oscillations Related to Sensorimotor Integration and Spatial Learning , 2003, The Journal of Neuroscience.

[14]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[15]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[16]  Werner Lutzenberger,et al.  Dynamics of gamma-band activity in human magnetoencephalogram during auditory pattern working memory , 2003, NeuroImage.

[17]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[18]  M. Kahana,et al.  Comparison of spectral analysis methods for characterizing brain oscillations , 2007, Journal of Neuroscience Methods.

[19]  Catherine Tallon-Baudry,et al.  Induced γ-Band Activity during the Delay of a Visual Short-Term Memory Task in Humans , 1998, The Journal of Neuroscience.

[20]  Itzhak Fried,et al.  Contrasting roles of neural firing rate and local field potentials in human memory , 2007, Hippocampus.

[21]  Gabriele Janzen,et al.  Selective neural representation of objects relevant for navigation , 2004, Nature Neuroscience.

[22]  Tony A. Fields,et al.  Cerebral microdialysis combined with single-neuron and electroencephalographic recording in neurosurgical patients. Technical note. , 1999, Journal of neurosurgery.

[23]  G McCarthy,et al.  Comparative localization of auditory comprehension by using functional magnetic resonance imaging and cortical stimulation. , 1999, Journal of neurosurgery.

[24]  E. Niebur,et al.  Neural Correlates of High-Gamma Oscillations (60–200 Hz) in Macaque Local Field Potentials and Their Potential Implications in Electrocorticography , 2008, The Journal of Neuroscience.

[25]  O Bertrand,et al.  Silence is golden: transient neural deactivation in the prefrontal cortex during attentive reading. , 2008, Cerebral cortex.

[26]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[27]  O. Bertrand,et al.  Neural correlates of consolidation in working memory , 2007, Human brain mapping.

[28]  G. Ojemann,et al.  Neurons in Human Temporal Cortex Active with Verbal Associative Learning , 1998, Brain and Language.

[29]  A. Walden,et al.  Spectral analysis for physical applications : multitaper and conventional univariate techniques , 1996 .

[30]  J. Winn,et al.  Brain , 1878, The Lancet.

[31]  M. Berger,et al.  High gamma activity in response to deviant auditory stimuli recorded directly from human cortex. , 2005, Journal of neurophysiology.

[32]  Hisao Nishijo,et al.  Representation of place by monkey hippocampal neurons in real and virtual translocation , 2003, Hippocampus.

[33]  Robert S. Astur,et al.  Factors affecting the hippocampal BOLD response during spatial memory , 2008, Behavioural Brain Research.

[34]  G Buzsáki,et al.  Cellular–Synaptic Generation of Sleep Spindles, Spike-and-Wave Discharges, and Evoked Thalamocortical Responses in the Neocortex of the Rat , 1997, The Journal of Neuroscience.

[35]  Karl J. Friston.  Testing for anatomically specified regional effects , 1997, Human brain mapping.

[36]  Charles L. Wilson,et al.  Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. , 2002, Journal of neurophysiology.

[37]  P M Thompson,et al.  Unfolding the human hippocampus with high resolution structural and functional MRI , 2001, The Anatomical record.

[38]  S. Raghavachari,et al.  Gating of Human Theta Oscillations by a Working Memory Task , 2001, The Journal of Neuroscience.

[39]  Erik Edwards.  Electrocortical activation and human brain mapping , 2007 .

[40]  Gary W. Van Hoesen.  The human parahippocampal region in Alzheimer’s disease, dementia, and ageing , 2002 .

[41]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[42]  D. Heeger,et al.  In this issue , 2002, Nature Reviews Drug Discovery.

[43]  T. Allison,et al.  Linking hemodynamic and electrophysiological measures of brain activity: evidence from functional MRI and intracranial field potentials. , 2004, Cerebral cortex.

[44]  V. Mountcastle.  The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[45]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[46]  Yevgeniy B. Sirotin,et al.  Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity. , 2009, Nature.

[47]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[48]  T. Allison,et al.  Comparison of cortical activation evoked by faces measured by intracranial field potentials and functional MRI: Two case studies , 1997, Human brain mapping.

[49]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

[50]  N. Logothetis,et al.  Neurophysiology of the BOLD fMRI Signal in Awake Monkeys , 2008, Current Biology.

[51]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[52]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[53]  Gabriel Curio,et al.  High-frequency (600 Hz) population spikes in human EEG delineate thalamic and cortical fMRI activation sites , 2008, NeuroImage.

[54]  Joshua E. Motelow,et al.  Negative BOLD with large increases in neuronal activity. , 2008, Cerebral cortex.

[55]  G Buzsáki,et al.  Sustained activation of hippocampal pyramidal cells by ‘space clamping’ in a running wheel , 1999, The European journal of neuroscience.

[56]  O. Jensen,et al.  Modulation of Gamma and Alpha Activity during a Working Memory Task Engaging the Dorsal or Ventral Stream , 2007, The Journal of Neuroscience.

[57]  Martin Lauritzen,et al.  Dissociation of spikes, synaptic activity, and activity-dependent increments in rat cerebellar blood flow by tonic synaptic inhibition , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Rajesh P. N. Rao,et al.  Spectral Changes in Cortical Surface Potentials during Motor Movement , 2007, The Journal of Neuroscience.

[59]  Edward O. Mann,et al.  Role of GABAergic inhibition in hippocampal network oscillations , 2007, Trends in Neurosciences.

[60]  D. Amaral,et al.  The Hippocampal Formation , 2009 .

[61]  Martin Wiesmann,et al.  Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging , 2004, NeuroImage.

[62]  I. Fried,et al.  Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex , 2005, Science.

[63]  R. Quian Quiroga,et al.  Unsupervised Spike Detection and Sorting with Wavelets and Superparamagnetic Clustering , 2004, Neural Computation.

[64]  Craig E. L. Stark,et al.  When zero is not zero: The problem of ambiguous baseline conditions in fMRI , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[65]  G. Buzsáki,et al.  Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks , 1995, Current Opinion in Neurobiology.

[66]  B. McNaughton,et al.  The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats , 1983, Experimental Brain Research.

[67]  Menno P. Witter,et al.  The parahippocampal region: past, present, and future , 2002 .

[68]  Arne D. Ekstrom,et al.  Correlation between BOLD fMRI and theta-band local field potentials in the human hippocampal area. , 2009, Journal of neurophysiology.

[69]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[70]  M M Haglund,et al.  Cerebral lateralization of neuronal activity during naming, reading and line-matching. , 1996, Brain research. Cognitive brain research.

[71]  B. McNaughton,et al.  Independence of Firing Correlates of Anatomically Proximate Hippocampal Pyramidal Cells , 2001, The Journal of Neuroscience.

[72]  R. Freeman,et al.  Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity , 2007, Nature Neuroscience.

[73]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

[74]  M. Mintun,et al.  Brain work and brain imaging. , 2006, Annual review of neuroscience.

[75]  G McCarthy.  Event-related potentials and functional MRI: a comparison of localization in sensory, perceptual and cognitive tasks. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[76]  K. Maravilla,et al.  Visualization-Based Mapping of Language Function in the Brain , 1997, NeuroImage.

[77]  G. Buzsáki.  Large-scale recording of neuronal ensembles , 2004, Nature Neuroscience.

[78]  G. Buzsáki,et al.  Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  Dae-Shik Kim,et al.  Origin of Negative Blood Oxygenation Level—Dependent fMRI Signals , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[80]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

[81]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[82]  David Corina,et al.  The roles of human lateral temporal cortical neuronal activity in recent verbal memory encoding. , 2009, Cerebral cortex.

[83]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[84]  R. Shapley,et al.  LFP power spectra in V1 cortex: the graded effect of stimulus contrast. , 2005, Journal of neurophysiology.

[85]  G. Ojemann,et al.  Anatomic subdivisions in human temporal cortical neuronal activity related to recent verbal memory , 2002, Nature Neuroscience.

[86]  K. Kubota,et al.  Cortical Mapping of Gait in Humans: A Near-Infrared Spectroscopic Topography Study , 2001, NeuroImage.

[87]  N. Logothetis,et al.  Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1 , 2006, Nature Neuroscience.

[88]  O. Bertrand,et al.  Relationship between task‐related gamma oscillations and BOLD signal: New insights from combined fMRI and intracranial EEG , 2007, Human brain mapping.

[89]  N Burgess,et al.  Unilateral temporal lobectomy patients show lateralized topographical and episodic memory deficits in a virtual town. , 2001, Brain : a journal of neurology.

[90]  Arne D. Ekstrom,et al.  High-resolution depth electrode localization and imaging in patients with pharmacologically intractable epilepsy. , 2008, Journal of neurosurgery.

[91]  J. Pernier,et al.  Induced gamma-band activity during the delay of a visual short-term memory task in humans. , 1998, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[92]  G A Ojemann,et al.  Neuronal recordings in human lateral temporal lobe during verbal paired associate learning. , 1995, Neuroreport.

[93]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[94]  W H Calvin,et al.  Human cortical neurons in epileptogenic foci: comparison of inter-ictal firing patterns to those of "epileptic" neurons in animals. , 1973, Electroencephalography and clinical neurophysiology.

[95]  Andrew P. Yonelinas,et al.  The intersubject and intrasubject reproducibility of FMRI activation during three encoding tasks: implications for clinical applications , 2006, Neuroradiology.

[96]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[97]  Martin Lauritzen,et al.  Brain Function and Neurophysiological Correlates of Signals Used in Functional Neuroimaging , 2003, The Journal of Neuroscience.

[98]  H. Duvernoy,et al.  The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI , 1997 .

[99]  M. Steriade,et al.  Focal synchronization of ripples (80-200 Hz) in neocortex and their neuronal correlates. , 2001, Journal of neurophysiology.

[100]  R. T. Constable,et al.  Neural correlates of temporal-order judgments versus those of spatial-location: Deactivation of hippocampus may facilitate spatial performance , 2005, Brain and Cognition.

[101]  Catherine Tallon-Baudry,et al.  The many faces of the gamma band response to complex visual stimuli , 2005, NeuroImage.

[102]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[103]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[104]  B. H. Bland,et al.  Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration , 2001, Behavioural Brain Research.

[105]  E. Maguire,et al.  The Well-Worn Route and the Path Less Traveled Distinct Neural Bases of Route Following and Wayfinding in Humans , 2003, Neuron.

[106]  F. Dudek,et al.  Intracellular correlates of fast (>200 Hz) electrical oscillations in rat somatosensory cortex. , 2000, Journal of neurophysiology.

[107]  P. König,et al.  A comparison of hemodynamic and neural responses in cat visual cortex using complex stimuli. , 2004, Cerebral cortex.

[108]  U. Mitzdorf.  Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[109]  R. Lemon,et al.  EEG oscillations at 600 Hz are macroscopic markers for cortical spike bursts , 2003, The Journal of physiology.

[110]  Marc W Howard,et al.  Gamma oscillations correlate with working memory load in humans. , 2003, Cerebral cortex.