Cross Laminar Traveling Components of Field Potentials due to Volume Conduction of Non-Traveling Neuronal Activity in Macaque Sensory Cortices

Abstract

Field potentials (FPs) reflect neuronal activities in the brain, and often exhibit traveling peaks across recording sites. While traveling FPs are interpreted as propagation of neuronal activity, not all studies directly reveal such propagating patterns of neuronal activation. Neuronal activity is associated with transmembrane currents that form dipoles and produce negative and positive fields. Thereby, FP components reverse polarity between those fields and have minimal amplitudes at the center of dipoles. Although their amplitudes could be smaller, FPs are never flat even around these reversals. What occurs around the reversal has not been addressed explicitly, although those are rationally in the middle of active neurons. We show that sensory FPs around the reversal appeared with peaks traveling across cortical laminae in macaque sensory cortices. Interestingly, analyses of current source density did not depict traveling patterns but lamina-delimited current sinks and sources. We simulated FPs produced by volume conduction of a simplified 2 dipoles' model mimicking sensory cortical laminar current source density components. While FPs generated by single dipoles followed the temporal patterns of the dipole moments without traveling peaks, FPs generated by concurrently active dipole moments appeared with traveling components in the vicinity of dipoles by superimposition of individually non-traveling FPs generated by single dipoles. These results indicate that not all traveling FP are generated by traveling neuronal activity, and that recording positions need to be taken into account to describe FP peak components around active neuronal populations.SIGNIFICANCE STATEMENT Field potentials (FPs) generated by neuronal activity in the brain occur with fields of opposite polarity. Likewise, in the cerebral cortices, they have mirror-imaged waveforms in upper and lower layers. We show that FPs appear like traveling across the cortical layers. Interestingly, the traveling FPs occur without traveling components of current source density, which represents transmembrane currents associated with neuronal activity. These seemingly odd findings are explained using current source density models of multiple dipoles. Concurrently active, non-traveling dipoles produce FPs as mixtures of FPs produced by individual dipoles, and result in traveling FP waveforms as the mixing ratio depends on the distances from those dipoles. The results suggest that not all traveling FP components are associated with propagating neuronal activity.

Keywords: cortical layer; current source density; local field potential; macaque; traveling wave; volume conduction.

Figure 1.

Laminar profiles of auditory FP responses. A, FP responses to 100 ms BF tone at an exemplar penetration site in primary auditory cortex. Top to bottom traces represent superficial to deep channels (1-23). Magenta and cyan dots label positive and negative peak components, respectively, that occurred during sounds at all channels. Vertical dotted line indicates the timing of P1 latency at channel 1. B, Laminar distributions of the peak latency of positive (magenta) and negative (cyan) FP components. Gray line (axis on top) indicates the laminar distribution of current sink peaks in granular layer plotted against the aligned depth. C, Laminar distributions of the normalized peak amplitude of positive (magenta) and negative (cyan) FP components. B, C, Mean (n = 95) and 95% simultaneous confidence bands are plotted against depth.

Figure 2.

Laminar profiles of auditory CSD responses. A, CSD responses to 100 ms BF tone at the same site as Figure 1A. Top to bottom traces represent superficial to deep channels (2-22). Magenta and cyan dots label positive and negative peak components, respectively. B, Laminar distribution of the peak latency of positive (magenta) and negative (cyan) CSD components (mean and 95% simultaneous confidence bands) is plotted against depth. C, D, Plot of median (n = 95) rate of change of the peak latency per a channel step (100 mm) against relative depth for the positive peaks (C) and negative peaks (D).

Figure 3.

Laminar profile of vcFP. A, vcFP of CSD responses shown in Figure 2A. Magenta and cyan dots represent positive and negative peak components, respectively, that occurred during sounds at all channels. Vertical dotted line indicates the P1 latency of original FP at channel 1 (same as that in Fig. 1). B, Mean peak latency of positive (magenta) and negative (cyan) components of vcFP. C, Plot of mean scores of the similarity of temporal patterns between FP and CSD (gray) and vcFP (black) against relative depth. Dotted lines indicate 95% simultaneous confidence bands.

Figure 4.

The effect of the relative peak timing of two dipole moments on vcFP. A, Left, Spatiotemporal profiles of CSD consisting of 2 dipoles at different depths and of same peak amplitudes. The onset of one dipole moment activation is delayed from another by 25 ms. Middle, Temporal patterns of vcFP derived from CSD in left column. Colors represent different depths. Insets (top of rows), Waveforms of two dipole moments (black represents early dipole; gray represents delayed dipole). Right, Spatiotemporal profiles of vcFP. White line indicates negative peak latency. Horizontal arrowheads indicate the positions of the polarity reversal of vcFP generated by individual dipoles. Left and right columns, Horizontal dotted lines indicate the positions of the centers of dipoles, and vertical dotted lines indicate the peak latencies of dipole moments. B–D, The onset delay of late dipole activation was gradually shortened from B to D (10 ms in B, 5 ms in C, and 0 ms in D). Other formats are the same as in A. C, D, Right column, Horizontal arrows indicate the delays of vcFP-negative peak components from the peak latency of late dipole moments. D, Right, Vertical arrowheads indicate temporal deviation between early dipole's peak latency and vcFP-negative peak latency at deep positions. Color scalebars for left and right columns, and legend for middle column are at bottom.

Figure 5.

The effect of the relative magnitudes of two dipole activities on vcFP. Two dipoles have the same spatiotemporal patterns as that in Figure 4D, with altered ratio of the amplitudes of early dipole moment to late dipole moment. Ratios are 8 (A), 2 (B), 0.5 (C), and 0.125 (D). Formats of left, middle, and right columns are the same as those in Figure 4. In right column, additional black lines indicate positive peak latency.

Figure 6.

Consequences of volume conduction with multiple dipoles. A, Plot of supragranular source peak latency against P1 peak latency (n = 95). B, Plot of traveling velocity of negative peaks against the velocity assumed for single dipoles generating both P1 and N1 (n = 95). B, Axes are scaled logarithmically.

Figure 7.

Dependence of the peak latency on the depth relative to polarity reversal. A, Peak latency of negative FP component at the depth of maximum MUA responses is plotted against the vertical distance of the depth from the polarity reversal of FP. B, Peak latency of negative CSD component at same depths, derived as in Figure 2B, is plotted against the vertical distance as in A. A, B, Straight lines indicate linear regression (n = 95).

Figure 8.

Laminar profile of occipital visual FP to red flashes. A, FP responses to red flashes at an exemplar penetration site in primary visual cortex. Top to bottom traces represent FP recorded at superficial to deep channels (1-23). Black dots label N1 for channel 1 and negative components whose peak latencies were closest to the peak latencies of negative components at channels one above. B, Mean and 95% confidence bands of peak latency of negative components of FP responses to red flashes are plotted against depth relative to the depth of inversions (n = 78). Gray line (axis on top) indicates the distribution of current sink peaks in granular layer.