How local is the local field potential?
- Authors
- Kajikawa, Yoshinao; Schroeder, Charles E
- Year
- 2011
- Journal
- Neuron
- PMID
- 22153379
- DOI
- 10.1016/j.neuron.2011.09.029
- PMCID
- PMC3240862
Local field potentials (LFPs) are of growing importance in neurophysiological investigations. LFPs supplement action potential recordings by indexing activity relevant to EEG, magnetoencephalographic, and hemodynamic (fMRI) signals. Recent reports suggest that LFPs reflect activity within very small domains of several hundred micrometers. We examined this conclusion by comparing LFP, current source density (CSD), and multiunit activity (MUA) signals in macaque auditory cortex. Estimated by frequency tuning bandwidths, these signals' "listening areas" differ systematically with an order of MUAΒ < CSDΒ < LFP. Computational analyses confirm that observed LFPs receive local contributions. Direct measurements indicate passive spread of LFPs to sites more than a centimeter from their origins. These findings appear to be independent of the frequency content of the LFP. Our results challenge the idea that LFP recordings typically integrate over extremely circumscribed local domains. Rather, LFPs appear as a mixture of local potentials with "volume conducted" potentials from distant sites.
Laminar patterns of auditory responses of LFP, CSD and MUA in the auditory cortexResponses to the BF tone in one example A1 site. Line plots (A) show LFP responses recorded at 23 depths using a linear array multielectrode with 100 ΞΌm intercontact spacing (schematic on left). In center (B) is the color plots of the laminar LFP profile shown in A; with negative deflection colored red and positive deflections colored blue. (C) depicts the CSD profile derived by the second derivative approximation of the field potential profile in A and B; red depicts extracellular current sinks (associated with net local inward transmembrane current flow) and blue depicts extracellular current sources (associated with net local outward transmembrane current flow). Selected MUA responses from channels 2, 6, 10, 15, and 19 are superimposed on the CSD plot. Vertical thin lines in all columns indicate stimulus onset. In this example, the peak of MUA at channel 15 corresponded to the peak negativity of LFP and current sink (CSD) at the response onset in Layer 4, and the responses from this location were used for analyzing lateral spread of signals. The asterisk indicates a superficial sink that produced N50.
Time courses of responses to tonesTone-evoked MUA, CSD and LFP responses at two example sites (A and B). MUA, CSD and LFP responses are colored blue, green and red, respectively. All time-bases extend from β30 to 170 ms relative to the onset of 100 ms duration tones, whose onsets and offsets are indicated by vertical dotted lines. Tone frequencies are indicated on the top row (kHz).
Normalized tuning curves for MUA, CSD and LFP(A and B) tuning curves of two exemplars shown in Figure 2. Colors of curves correspond to MUA (blue), CSD (green) and LFP (red). (C) Summary of tuning curves across all penetration sites. Line and dotted line traces represent the median and its 95% confidence intervals of all recording sites (n=130). The MUA, CSD and LFP tuning curves of the individual sites were shifted on the frequency axis to align the best frequencies of MUA tuning curves on zero. (D) Boxplot showing the median and the first and third quartiles of BWMUA (blue), BWCSD (green) and BWLFP (red).
Comparisons of LFPobs and LFPcal(A) Laminar-temporal profiles (β30 β 170 ms) of LFPobs, CSD, LFPcal responses, and disparity of signs between LFPobs and LFPcal (from left to right) responses to tones of frequencies from 0.35 kHz (top) to 32 kHz (bottom) of one example recording site. In the first to third columns, red and blue correspond to negative and positive polarities, respectively. In the forth column, red indicates positions of unequal polarity (Ξsign) between laminar-temporal profiles of LFPobs and LFPcal responses. White vertical lines indicate the onset and offset of tones. (B) Tuning curves (blue: MUA, green: CSD, red: LFPobs) of the example site shown in A, with SXCorr (black) overlain over tone frequencies (see text for details). (C) Summary of SXCorr curves across penetration sites. Line and dotted line curves represent the median and its 95% confidence intervals estimated from all penetration sites (n=130).
Spread of auditory LFP responses perpendicular to the auditory cortex(A) Profile of auditory LFP responses to 100 ms BBN stimulus measured during an electrode penetration from the dura down through the depth of auditory cortex (schematic of the penetration depicted on a brain coronal section at the left; inset shows that approximate position and angle of the section). Gray vertical line indicates stimulus onset. Black vertical line indicates the timing 24 ms post onset of stimuli, used to derive the amplitude profiles. Inset shows expanded view of top one third depths, and same applies to two other columns (B and C). (B) The distribution of the amplitude of LFP (red) and CSD (blue) signals at 24 ms for the example shown in A. The origin of the vertical axis is set to the depth of inversion of polarity within the auditory cortex. (C) Distribution of median of normalized amplitudes at 24 ms (n=105). Normalization was done with respect to the mean absolute amplitudes of all depths for each penetration site. For each track, recording depths were rounded to depths with intervals of 0.5 mm and mean amplitudes of multiple depths rounded to each step were used. Split lines show 95 % confidence intervals of median. On the left, a coronal section of Nissl stained brain is shown to illustrate the electrode track. (LS, lateral sulcus; STS, superior temporal sulcus; 3B; somatosensory area 3B; S2, secondary somatosensory cortex; RI, retroinsular cortex; STP, superior temporal polysensory area)
Spread of frequency bands of LFP responses(A) The median amplitude distributions of band-limited signals of auditory LFP responses to BBN (n =105). Panels from left to right show amplitudes of frequency bands (FB1: 1~2.9 Hz, FB2: 3~8.8 Hz, FB3: 9.1~26.7 Hz, FB4: 27.7~81 Hz, FB5: 83.9~256 Hz) at the time of 24 ms post stimulus onset. Amplitudes were normalized with respect to the mean absolute amplitudes of all depths for each penetration site. Asterisks indicate depths where median normalized amplitudes did not significantly differ from zero according to 95 % confidence intervals (bootstrap). Gray crosses label depths where phases of signals were random between penetration sites. Other format conventions are the same as Figure 5C. (B) The median power distributions of band-limited signals of auditory LFP responses. Panels from left to right show increments of power at 24 ms post onset of stimuli from the prestimulus baseline for 5 FB at distances relative to the depth of inversion. In all panels, dashed lines indicate the 95% confidence intervals of median amplitude distributions.
Tuning curves after subtraction of the mean for CSD and LFP(A) Summary of tuning curves of MUA (blue), CSD (green) and LFP (red) across all experiments. Line and dotted line traces represent the median and its 95% confidence intervals (bootstrap, n=130). Tuning curves were normalized to their peaks after subtracting their mean values. MUA tuning curves are the same as those shown in Fig. 1C. (B) Boxplot showing the median and the first and third quartiles (n=130) of BWMUA (blue), BWCSD (green) and BWLFP (red). BWCSD and BWLFP were derived after subtraction of mean values.
| # | Section | Preview |
|---|---|---|
| 40 | Discussion β Summary and Conclusions | This study evaluated the recent proposition that LFP recordings generally sample over an extremelyβ¦ |
| 41 | Experimental Procedures β Subjects, stimuli and recordings | All procedures were approved by the IACUC of the Nathan Kline Institute. Recordings were made in sixβ¦ |
| 42 | Experimental Procedures β Analyses | LFP and MUA signals were averaged across trials. CSD was calculated from LFPs by numericalβ¦ |
| 43 | Experimental Procedures β Volume conduction | We analyzed the relationship between LFP and CSD signals based on theoretical arguments describedβ¦ |
| 44 | Experimental Procedures β Volume conduction | A straightforward interpretation would be that it describes electrical potential at the position,β¦ |
| 45 | Experimental Procedures β Volume conduction | al., 2007). In this study, we substituted CSD signals for q(rβ) to calculate a spatial LFPβ¦ |
| Name | Type |
|---|---|
| action potentials local | drug |
| anesthetics | drug |
| anesthetized subjects local | cohort |
| auditory cortex | anatomy |
| Auditory LFP local | phenotype |
| awake macaques local | cohort |
| awake subjects local | cohort |
| BBN local | drug |
| BFMUA local | anatomy |
| binaural auditory stimuli local | drug |
| brain surface local | anatomy |
| broad-band noise local | drug |
| Broadband noise local | drug |
| cortex | anatomy |
| cortical sheet | anatomy |
| CSD | drug |
| CSD analysis local | drug |
| Current source density local | phenotype |
| dorsal brain surface local | anatomy |
| dorsal surface of brain local | anatomy |
| dura | anatomy |
| EEG | phenotype |
| epidural brain surface local | anatomy |
| ERP | phenotype |
| event-related potential local | drug |
| excitatory postsynaptic potential (EPSP) local | drug |
| Extracellular current sinks/sources local | phenotype |
| Extracellular potential local | phenotype |
| Generator substrates local | phenotype |
| Givre et al., 1994 local | cohort |
| granule cell local | anatomy |
| high stimulus frequencies local | phenotype |
| inferior bank of the lateral sulcus local | anatomy |
| infragranular layers local | anatomy |
| intracranial recording local | phenotype |
| inversion | variant |
| Ionic conductance states local | phenotype |
| isotropic conductivity local | phenotype |
| Katzner et al. (2009) local | cohort |
| Katzner et al., 2009 local | cohort |
| Layer 3 local | anatomy |
| layer 4 local | anatomy |
| Layer 4 local | anatomy |
| LFP | phenotype |
| LFPcal local | anatomy |
| LFPcal local | drug |
| LFPcal local | phenotype |
| LFP negativity local | phenotype |
| LFPobs local | anatomy |
| LFPobs local | drug |
| LFPobs local | phenotype |
| LFP response local | drug |
| linear array multielectrodes local | drug |
| local field potential | drug |
| local field potential (LFP) local | drug |
| low frequencies local | phenotype |
| Maier et al., 2011 local | cohort |
| membrane capacitance | phenotype |
| membrane potential | phenotype |
| Mitzdorf and Singer, 1978 local | cohort |
| monkeys | cohort |
| MUA local | anatomy |
| MUA local | drug |
| MUA | phenotype |
| multi-unit activity (MUA) local | drug |
| N50 local | phenotype |
| negative deflection local | phenotype |
| neocortex | anatomy |
| Neuronal substrate local | anatomy |
| nonhuman animals local | cohort |
| P30 local | phenotype |
| P30 component local | phenotype |
| penetration site local | anatomy |
| Peterson et al., 1995 local | cohort |
| Poisson's differential equation local | drug |
| Poisson's equation local | drug |
| polarity-depth invariance local | phenotype |
| polarity inversions local | phenotype |
| primary auditory cortex | anatomy |
| primary auditory cortex (A1) local | anatomy |
| primary sensory cortices local | anatomy |
| primary visual cortex | anatomy |
| reference electrodes local | drug |
| scalp | anatomy |
| Schroeder1995 Study local | cohort |
| Secondary Somatosensory Cortex local | anatomy |
| Steinschneider et al., 2008 local | cohort |
| Superior Temporal Sulcus local | anatomy |
| supragranular A1 local | anatomy |
| supragranular layers local | anatomy |
| Supragranular layers local | anatomy |
| synaptic activity | phenotype |
| synaptic processes | phenotype |
| tone | drug |
| tone (60 dB, 100 ms) local | drug |
| tonotopic gradient local | phenotype |
| Transmembrane current local | phenotype |
| typical LFP local | phenotype |
| volume conduction local | phenotype |
| volume conduction effects local | phenotype |
| Xing et al. local | cohort |
| Xing et al. (2009) local | cohort |
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