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Neuronal correlates of functional magnetic resonance imaging in human temporal cortex.

Ojemann GA, Corina DP, Corrigan N, Schoenfield-McNeill J, Poliakov A, Zamora L, Zanos S - Brain (2009)

Bottom Line: 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.Neither analysis provided evidence for an independent relation to frequency of single neuron activity.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurological Surgery, Campus Box 356470, University of Washington, 1959 NE Pacific Street, Seattle, WA 98195, USA. gojemann@u.washington.edu

ABSTRACT
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.

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Single neuron activity recorded simultaneously from sites 20 and 21 of Subject 506. (A) Frequency of single neuron activity recorded from each site during the two blocks each with PA and associated fixation, and the interspersed block of ID and associated fixation. Inset in each block's data is the average waveform of the action potentials recorded during that block. Bar in that insert is 2 ms. The activity illustrated for each block is the average of the eight cycles of fixation and behaviour in 100 ms bins, with the red line dividing the equal 21 s periods of fixation or behaviour. Bar below each block is the 1.3 s duration of an individual item in behavioural portion, and equivalent segment of fixation, expanded into individual item peristimulus time histograms in Figure 3. (B) Average frequency of single neuronal firing for each condition. Site 20 blue, 21 green. The fMRI had significantly increased activity for two comparisons, PA fixation and [(PA–PA fixation) – (ID–ID fixation)] at site 21, and significantly reduced activity for all three comparisons at site 20. The change in average single neuron firing rates at both sites is shown for the two comparisons with significant fMRI changes at both sites, increases at site 21 and decreases at site 20. (C) Difference in average firing rates between PA compared with PA fixation. Site 20 blue, 21 green. Asterisk above bar, significant change at P < 0.025. Asterisk below pair, significant difference between sites at P < 0.025. (D) Difference in average firing rate for [(PA–PA fixation) − (ID–ID fixation)] comparison, presented as in C. As indicated by the consistent action potential waveforms at each site, stable single neuron activity was recorded throughout the blocks. In this patient, there is increased average activity during ID at both sites, compared with ID fixation. However, activity during PA shows a differential response: greater activity for PA compared with PA fixation at site 21, less activity with PA at site 20. The increase in neuronal firing at site 21 is significant for only one of the two comparisons that had significant fMRI signal increases at this site, while significantly decreased neuron firing occurred at site 20 on both comparisons, both of which also had significant fMRI signal decrease at this site.
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Figure 2: Single neuron activity recorded simultaneously from sites 20 and 21 of Subject 506. (A) Frequency of single neuron activity recorded from each site during the two blocks each with PA and associated fixation, and the interspersed block of ID and associated fixation. Inset in each block's data is the average waveform of the action potentials recorded during that block. Bar in that insert is 2 ms. The activity illustrated for each block is the average of the eight cycles of fixation and behaviour in 100 ms bins, with the red line dividing the equal 21 s periods of fixation or behaviour. Bar below each block is the 1.3 s duration of an individual item in behavioural portion, and equivalent segment of fixation, expanded into individual item peristimulus time histograms in Figure 3. (B) Average frequency of single neuronal firing for each condition. Site 20 blue, 21 green. The fMRI had significantly increased activity for two comparisons, PA fixation and [(PA–PA fixation) – (ID–ID fixation)] at site 21, and significantly reduced activity for all three comparisons at site 20. The change in average single neuron firing rates at both sites is shown for the two comparisons with significant fMRI changes at both sites, increases at site 21 and decreases at site 20. (C) Difference in average firing rates between PA compared with PA fixation. Site 20 blue, 21 green. Asterisk above bar, significant change at P < 0.025. Asterisk below pair, significant difference between sites at P < 0.025. (D) Difference in average firing rate for [(PA–PA fixation) − (ID–ID fixation)] comparison, presented as in C. As indicated by the consistent action potential waveforms at each site, stable single neuron activity was recorded throughout the blocks. In this patient, there is increased average activity during ID at both sites, compared with ID fixation. However, activity during PA shows a differential response: greater activity for PA compared with PA fixation at site 21, less activity with PA at site 20. The increase in neuronal firing at site 21 is significant for only one of the two comparisons that had significant fMRI signal increases at this site, while significantly decreased neuron firing occurred at site 20 on both comparisons, both of which also had significant fMRI signal decrease at this site.

Mentions: As illustrated in Fig. 2 for the two recording sites in one subject, well-isolated single neuron activity with stable waveforms throughout the various blocks was recorded. The frequency of single neuron activity simultaneously recorded from two sites (20, 21) in the illustrative subject during the two blocks of PA and interposed ID block is also indicated. The location of those two recording sites is shown in Fig. 1. The changes in average activity for the two comparisons that had significant changes in fMRI signal at both sites, decreased fMRI activity at site 20 and increased at site 21, are also illustrated.Figure 2


Neuronal correlates of functional magnetic resonance imaging in human temporal cortex.

Ojemann GA, Corina DP, Corrigan N, Schoenfield-McNeill J, Poliakov A, Zamora L, Zanos S - Brain (2009)

Single neuron activity recorded simultaneously from sites 20 and 21 of Subject 506. (A) Frequency of single neuron activity recorded from each site during the two blocks each with PA and associated fixation, and the interspersed block of ID and associated fixation. Inset in each block's data is the average waveform of the action potentials recorded during that block. Bar in that insert is 2 ms. The activity illustrated for each block is the average of the eight cycles of fixation and behaviour in 100 ms bins, with the red line dividing the equal 21 s periods of fixation or behaviour. Bar below each block is the 1.3 s duration of an individual item in behavioural portion, and equivalent segment of fixation, expanded into individual item peristimulus time histograms in Figure 3. (B) Average frequency of single neuronal firing for each condition. Site 20 blue, 21 green. The fMRI had significantly increased activity for two comparisons, PA fixation and [(PA–PA fixation) – (ID–ID fixation)] at site 21, and significantly reduced activity for all three comparisons at site 20. The change in average single neuron firing rates at both sites is shown for the two comparisons with significant fMRI changes at both sites, increases at site 21 and decreases at site 20. (C) Difference in average firing rates between PA compared with PA fixation. Site 20 blue, 21 green. Asterisk above bar, significant change at P < 0.025. Asterisk below pair, significant difference between sites at P < 0.025. (D) Difference in average firing rate for [(PA–PA fixation) − (ID–ID fixation)] comparison, presented as in C. As indicated by the consistent action potential waveforms at each site, stable single neuron activity was recorded throughout the blocks. In this patient, there is increased average activity during ID at both sites, compared with ID fixation. However, activity during PA shows a differential response: greater activity for PA compared with PA fixation at site 21, less activity with PA at site 20. The increase in neuronal firing at site 21 is significant for only one of the two comparisons that had significant fMRI signal increases at this site, while significantly decreased neuron firing occurred at site 20 on both comparisons, both of which also had significant fMRI signal decrease at this site.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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Figure 2: Single neuron activity recorded simultaneously from sites 20 and 21 of Subject 506. (A) Frequency of single neuron activity recorded from each site during the two blocks each with PA and associated fixation, and the interspersed block of ID and associated fixation. Inset in each block's data is the average waveform of the action potentials recorded during that block. Bar in that insert is 2 ms. The activity illustrated for each block is the average of the eight cycles of fixation and behaviour in 100 ms bins, with the red line dividing the equal 21 s periods of fixation or behaviour. Bar below each block is the 1.3 s duration of an individual item in behavioural portion, and equivalent segment of fixation, expanded into individual item peristimulus time histograms in Figure 3. (B) Average frequency of single neuronal firing for each condition. Site 20 blue, 21 green. The fMRI had significantly increased activity for two comparisons, PA fixation and [(PA–PA fixation) – (ID–ID fixation)] at site 21, and significantly reduced activity for all three comparisons at site 20. The change in average single neuron firing rates at both sites is shown for the two comparisons with significant fMRI changes at both sites, increases at site 21 and decreases at site 20. (C) Difference in average firing rates between PA compared with PA fixation. Site 20 blue, 21 green. Asterisk above bar, significant change at P < 0.025. Asterisk below pair, significant difference between sites at P < 0.025. (D) Difference in average firing rate for [(PA–PA fixation) − (ID–ID fixation)] comparison, presented as in C. As indicated by the consistent action potential waveforms at each site, stable single neuron activity was recorded throughout the blocks. In this patient, there is increased average activity during ID at both sites, compared with ID fixation. However, activity during PA shows a differential response: greater activity for PA compared with PA fixation at site 21, less activity with PA at site 20. The increase in neuronal firing at site 21 is significant for only one of the two comparisons that had significant fMRI signal increases at this site, while significantly decreased neuron firing occurred at site 20 on both comparisons, both of which also had significant fMRI signal decrease at this site.
Mentions: As illustrated in Fig. 2 for the two recording sites in one subject, well-isolated single neuron activity with stable waveforms throughout the various blocks was recorded. The frequency of single neuron activity simultaneously recorded from two sites (20, 21) in the illustrative subject during the two blocks of PA and interposed ID block is also indicated. The location of those two recording sites is shown in Fig. 1. The changes in average activity for the two comparisons that had significant changes in fMRI signal at both sites, decreased fMRI activity at site 20 and increased at site 21, are also illustrated.Figure 2

Bottom Line: 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.Neither analysis provided evidence for an independent relation to frequency of single neuron activity.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurological Surgery, Campus Box 356470, University of Washington, 1959 NE Pacific Street, Seattle, WA 98195, USA. gojemann@u.washington.edu

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus