Bit-mapped color imaging of human evoked potentials with reference to the N20, P22, P27 and N30 somatosensory responses

Bit-mapped color imaging of human evoked potentials with reference to the N20, P22, P27 and N30 somatosensory responses

Electroencephalography and clinical Neurophysiology, 1987, 68:1-19 Elsevier Scientific Publishers Ireland, Ltd. EEG 01883 Bit-mapped color imaging o...

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Electroencephalography and clinical Neurophysiology, 1987, 68:1-19 Elsevier Scientific Publishers Ireland, Ltd.

EEG 01883

Bit-mapped color imaging of human evoked potentials with reference to the N20, P22, P27 and N30 somatosensory responses John E. Desmedt, Tran Huy Nguyen and Marc Bourguet Brain Research Unit, "Unit~ersjtyof Brussels, Brussels 1000 (Belgium)

(Accepted for publication: 30 September, 1986)

Summary

Bit-mappedcolor imaging of scalp potential fields evoked by sensory stimulation in humans disclosed significant features not identified by mereinspection of multichannel traces. Methodologicalproblems are considered in detail for early cortical SEPs which include several components with sharp rise times occurring at spatially distinct scalp locations. A manageable yet efficient imaging system requires recording electrodes in adequate number and scalp locations, bandpass fidelity to resolve slow and fast components, consistencyof bioelectric input data, optimal interpolation and mapping algorithms, and consistent color scaling. Critical steps in these procedures were investigated in conjunctionwith new evidence on the scalp topographyand neural generators of the N20, P20, P22, P27 and N30 SEP components. It is concluded that N20-P20 reflect a tangential equivalent dipole in parietal area 3b while P22 reflects a radial equivalent dipole in motor area 4. Key words: topographicmapping; somatosensoryevoked potentials; man; averagingprocedure; cortical dipole generators; motor cortex response

Scalp evoked potential (EP) wave forms to a transient sensory stimulus are no longer thought to merely reproduce fluctuations of soma-dendritic membrane potentials in neurons of the receiving areas of sensory cortex (Creuzfeldt et al. 1969), but rather viewed as composite profiles made up of distinct components that reflect activation of different neurons in the afferent pathway (far-field components) or cortex (nearfield components) (Desmedt 1971, 1984; Jewett and Williston 1971; Cracco and Cracco 1976; King and Green 1979; Chiappa et al. 1980; Desmedt and Cheron 1980a, 1981a; Anziska and Cracco 1981; Eisen 1982; Kimura et al. 1983; Lueders et al. 1983; Mauguifre et al. 1983b; Yamada et al. 1983). For meaningful use of EPs in

Correspondence to: Prof. J.E. Desmedt, Brain Research Unit, 115 Boulevard de Waterloo, 1000 Brussels, Belgium. 1 This research was supported by the Fonds de la Recherche Scientifique M~dicale, Belgium.

brain research or clinical diagnosis, the brain locations and time features of neural generators of each component should be identified. Since no single electrode montage can disclose all pertinent EP components (Goff et al. 1962; Desmedt and Cheron 1980b), it has been necessary to use multichannel recordings which are best investigated through topographic mapping of EP fields (Duffy et al. 1978; Ragot and R f m o n d 1978; Lehmann and Skrandies 1980; Coppola et al. 1982; Desmedt and Nguyen 1984; Thickbroom et al. 1984; Desmedt and Bourguet 1985; Giard et al. 1985; Nuwer 1985; Deiber et al. 1986). A m o n g EPs, the somatosensory EPs (SEPs) present unusual opportunities for mapping the different near-field components because of the deployment of several somatosensory cortical projection areas over the brain convexity right under the skull. This contrasts with the more deeply located auditory or visual receiving areas which are less readily analyzed in scalp recordings. Bit-mapped color imaging refers to raster dis-

0168-5597/87/$03.50 © 1987 Elsevier Scientific Publishers Ireland, Ltd.

2 play systems in which the displayable picture elements (pixel) are represented by a memory location in a refresh computer buffer. These recent methods enhance the visibility of significant EP features that are not readily perceived through mere inspection of multichannel traces. The early SEP response involves components with sharp rise times occurring at spatially distinct scalp locations with small shifts of latency (Desmedt and Bourguet 1985) which challenges the imaging system to come up with adequate temporal and spatial resolution. This paper describes methods for practical and efficient bit-mapped EP imaging in conjunction with new evidence on the topography and generators of the early cortical SEP components.

J.E. DESMEDTET AL. processor-based 4695 Tektronix ink-jet color graphics copier which bit-mapped at 120 dots/in. (about 14,000 dots/in. 2) in asynchronous dropon-demand mode. Each pixel of 1/30 in. was formed by 4 rows of 4 dots of chosen colors (black, cyan, magenta, yellow) as determined by computer commands. Width of graphic field was 1024 dots or 256 pixels. The local intelligence in the copier made the host computer task easier and faster. Component labels used P (positive) or N (negative) and modal peak latency in normal adults of standard body size (Donchin et al. 1977). To avoid inconsistencies in discussions, the labels of standard SEP components are now indeed used as a characteristic name (e.g., N20, P27) which does not have to reflect minor deviations of latencies in a particular study.

Material and methods

This report is based on SEPs studied in 15 paid volunteers of 19-34 years of either sexes, in good health, free from neurological disease and non-addicted to drugs. Mean body size was 175 cm. They gave informed consent. Selection was based on good yields in SEPs and ability to relax and minimize EMG and eyeblink interference. Awake subjects laid on a reclining chair in a soundproofed, electrically shielded and air-conditioned room at 24 ° C, separate from the instrument control room. Square electrical pulses of 0.2 msec were delivered by metal rings to one or more fingers (1 msec delay for thumb). Intensities set at 3 times sensory threshold were monitored throughout on nixies coupled to a peak A / D detector chip in the primary of stimulator's output transformer. Interstimulus intervals were 0.3-1.4 sec. Skin temperature of stimulated limb was 35 o C. Scalp potentials were recorded with thin stainless steel needles with impedance below 3 kI2. Twenty-eight high quality homemade differential (110 dB common mode rejection at 1 kHz) amplifiers were designed with low-noise dual FET input (MPS843, MicroPower Systems) followed by highly stable AD624 instrumentation amplifier chips (Analog Devices). Input impedance was 33 MI2. EEGs were monitored on a bank of SC501 Tektronix miniscopes. Color images were drawn on paper by micro-

Results and discussion

Data processing Scalp mapping requires consistent averaging of bioelectric data from all recording electrodes. Low-noise and precisely matched amplifiers should be used. Our system achieved a stable gain (20,000) that differed by less than _ 1% between channels (Fig. 7J-L) and also excluded channel asymmetries due to amplifier overload or interference. If any channel was blocked during a few trials of a run, its averaged voltage would be spuriously reduced as compared to signals in other channels which would distort potential fields in topograpic mapping. Faithful display of both relatively slow (N18, N30, P45) and fast (N20, P22, P27) SEP components requires amplifier bandpass from 2 kHz to 1.6 Hz and averaging sampling rate of 4 kHz or higher (Desmedt et al. 1974). This requirement raises problems for serial averaging with many channels. For example, the PDP 11-34 Digital computer (256 kbytes CPU, 2 RK06 disks) under R T l l operates sequential analog-to-digital (A/D) conversions through multiplexer and A D l l K converter whereby only 7 channels can be used at 4 kHz (bins 250/~sec) or 15 at 2 kHz. Such difficulties are eliminated by parallel processing which is a must for fast multichannel averaging.

BIT-MAPPED IMAGING OF SEP Our system was based on AD574-A converters (Analog Devices) operating 28 parallel A / D conversions (12 bits) in 15 ~tsec and data were averaged on-line. A D R l l W direct-access memory module (DMA) managed via K W l l K programmable clock accessed the bus to CPU memory. The 28 converters were connected to the bus via 3-state (high impedance) registers. Averaging involved for each data point: reading request to central memory for stored data value (maximum 4 /~sec), reading of A / D converter output, addition of the two, and writing request to CPU for storing updated data (which takes 200 nsec). A test of data conformity based on a double comparator checked for each input data whether the 8 higherweight bits did not exceed a chosen range. If any of the 28 output data from converter did so in a given trial, the addition process of all 28 channel data was disabled for that trial. This rejected from the average each trial in which any channel exceeded a predetermined fork of input potential (e.g., + 150/~V) thereby excluding mapping errors from amplifier overload and excess deviation from baseline. When appropriate, a separate electronic trigger circuit was used for surveillance of 1 or 2 most vulnerable channels in which transients such as cephalic muscle E M G occurred that did not transgress the above-mentioned fork threshold but were nevertheless annoying. Averaging/rejection took a maximum of 28 x 4.2--123 /xsec while A / D conversion took 30 /~sec for all channels. However each (n + 1)th conversion could be made to overlap the nth averaging writing cycle as the latter's operations were protected by the high-impedance state register between bus and converters output. The system was run at 8 kHz (bin 125/~sec) up to 28 channels or 4 kHz up to 56 channels.

Number and location of scalp electrodes Optimized EP mapping should negotiate practical solutions on the basis of several requirements. First, the number of channels should not exceed a manageable set (like the 21 or so in standard EEG), otherwise the time taken to set up and maintain adequate recording conditions becomes excessive. Second, both hemispheres should be recorded concomitantly to image EP fields that

3 extend across midline (Desmedt and Bourguet 1985) and recording only one hemisphere at a time (Coppola et al. 1982; Giard et al. 1985) is not sufficient. Third, for imaging the peak values of any potental field, an electrode must be near the field culmination since electrodes around that focal site only record smaller potentials (Duff 1980). This requires either using many electrodes (say, 64 up) or optimizing electrodes at focal sites. Fourth, the mapping algorithm should not impose restrictions like, for example, that scalp electrodes are evenly spaced which would prevent the desired flexibility in deciding electrode sites. These issues were studied by recording from 27 scalp electrodes at sites related to the 10-20 system with additional coronal rows of electrodes at 10% either in front or behind vertex (Fig. 1). The central coronal plane itself is critical for early SEP responses in the pericentral region (Desmedt and Cheron 1980b, 1981b). Anatomical correlations had shown the standard EEG C3 and C4 positions to usually overlap the precentral gyms, but sometimes also the postcentral gyrus in different subjects (Jasper 1958; Hellstr~Sm et al. 1964; Blume et al. 1974). Therefore, the central coronal row was shifted 1 or 1.5 cm in front of Cz to ensure that such C3' and C4' sites (20% from midline) overlapped the motor strip in front of the central fissure. The T3' and T4' sites (40% from midline) were also shifted forward even though they were not critical. In an attempt to limit the number of electrodes without loss of resolution (see below), 4 instead of 5 electrodes were used in the frontal or parietal coronal rows. For the latter, sites at 10 and 30% from midline proved indeed more useful than those at 20 and 40%. For prefrontal or occipital regions, two electrodes were placed at 20% (not 10%) above inion or nasion respectively and at 10% to left or right of midline (Fig. 1). Maps based on these 27 optimally placed electrodes served as reference base in any subject. Additional maps were computed by dropping data for particular electrodes from the set to assess their contribution to the array.

Mapping algorithms Following the 10-20 system, the head volume was represented on a single plane circular projec-

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between actual recording sites (Coppola et al. 1982). Electrode positions were expressed in polar coordinates by their latitude from central coronal axis and distance from Cz (as fraction of head radius in 10-20 system). Fig. 2 and Table I illustrate for the 4 quadrants how positions were expressed in cartesian coordinates Xm and Ym of the pixel matrix. When required, electrode coordinates were collapsed into the nearest pixel. The square matrix included 79 × 79 = 6241 pixels of which 4005 imaged the head map. This provided adequate detail (Fig. 5) while a matrix of 1000 pixels was clearly not acceptable (Fig. 7G-I). The head contour matrix was drawn 5% and color map 10% above nasion-inion level (Fig. 1A) to avoid extrapolations outside electrode array. The latter was adequate for mapping SEPs generated in parieto-frontal regions, but additional coverage of occipital regions would be required for VEPs. Several reference files served for map computation (Fig. 3). A file stored the square matrix with head contour and electrode positions in pixel coordinates (Fig. 2). Another saved, for each of the 4005 color pixels, the identification of the 4 (or

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tion with center at Cz (Jasper 1958). Interelectrode distances over the head were fairly proportional to distances between their representations in the two-dimensional circle. Especially for the region within about 7 cm from Cz on the top of the head (Rush and Driscoll 1968) where early cortical SEP components culminate, the potential gradient changes were consistent and a simple interpolation algorithm was used to fill in the map

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BIT-MAPPED I M A G I N G OF SEP

5

TABLE I Calculation of the electrode coordinates in 2-dimensional matrix for brain mapping. The polar coordinates are the angle from the central coronal plane (a in degrees) and the distance from Cz (b as fraction of head radius in the 10-20 system) (Fig. 2). Xp and Yp are the electrode coordinates in this polar coordinate system. Xm and Ym are expressed in the pixel matrix of Fig. 2. Position

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any chosen number) nearest electrodes and their proportional weights. These weights were calculated in inverse linear (or square, cubic) proportion to the distance from any pixel to each of the 4 nearest electrodes and scaled to decimal fractions totalling 1.0 (Table II). Computation of the voltage V of any pixel at any latency was as follows: V=A

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m nearest electrodes for interTABLE II Calculation of the voltage of the circled pixel of Fig. 10B with different interpolation algorithms involving the 4 or 6 nearest electrodes and different weighting of relative distances from pixel to the electrodes (dividing by distance or cubic power of distance). The data considered correspond to 14-channel mapping.

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6 after subtraction of a baseline that was estimated for each channel by averaging the signal for 10 msec before stimulus. Before reading the averaged data file, the map program called for selection of parameters such as number of channels, voltage scales, number of sequential maps (up to 60) and latency of each map after stimulus. Any latencies at 250 #sec increments could be chosen for imaging dynamic potential fields through series of frozen maps. After computing 4005 pixels at any given latency, the map program assigned them to appropriate voltage and color steps. The picture file was used for hardcopies.

Design of color displays The synthetic pigments, magenta, yellow and cyan, correspond to the 3 primary colors and are widely used for technical color printing. Mixing two of them in equal proportions produces the 3 secondary colors, orange, green and violet. Changing proportions in these mixtures results in many gradations or nuances. On a perception basis, colors are classified according to hue (the color true and proper), lightness (relation to white and black) and saturation (purity of color) (De Grandis 1986). For color hardcopying, each pixel formed by 4 × 4 matrix of dots of selected hues was produced by subtractive combination of dots of different colors. Lightness and saturation were set by half-toning, that is by having black and/or white dots intermixed. The pixel dot pattern was designed with appropriate geometries to produce various textures (stipple, lines of various thickness) to improve visual discrimination between voltage steps. The implementation algorithms used these parameters to appropriately scale hue and saturation in color labels, taking into account non-finearities of human color perception and the perceptual interactions between any given color and the surrounding colors.

Color coding of potential polarities The color convention is somewhat arbitrary but there are arguments to suggest a red-negative and blue-positive code rather than the reverse. First, color scales should be perceptually meaningful.

J.E. DESMEDTET AL. People generally see the spectral order as a natural one. Warm longer wave length colors (red) associate in the mind with sunlight and fire and tend to signify action. Cool shorter wave length colors (blue) associate with water and moonlight and are geen as less active and receding. Second, it is well known that neuronal excitation involves a negative potential shift in the extracellular space surrounding the depolarized membrane. Since all EPs (whether near-field or far-field) recorded at the skin are extracellular potentials, it is in principle more consistent to depict by warm red-yellows the scalp negativities in the nearfield. Blue is then used for positive potentials. As a choice has to be made for polarity coding, we think the proposed color convention makes more sense on general physiological principles. However, the argument cannot be used in reverse and it would be wrong to say that scalp-recorded EP positivities always imply reduced excitation at the generator considered. In fact, actual polarities at different scalp locations reflect not only levels of activation but also geometry of the corresponding neural generators in the volume conductor of the head. For example, epileptic spikes reflecting paroxystic activities are usually negative in the EEG near the focus. The cortical DC potential level goes more negative with arousal and less negative with relaxation or sleep onset (Rowland 1968; Skinner and Yingling 1977). Along the same line, the scalp-positive cognition-related P300 response largely reflects brain relaxation after a cognitive decision (Desmedt and Debecker 1979). On the other hand, ERP components reflecting brain processing before P300 are usualy negative like N100, N400 (Hillyard and Picton 1979; Ritter et al. 1979; Kutas and Hillyard 1980; N~i~it~inen1982; Renault et al. 1982) but can be positive like P40, P100 (Desmedt et al. 1983). Also, early cortical SEP components recorded right over the receiving areas can be either negative (N20) or positive (P22, P27) without there being any a priori reason that this would reflect opposite states of excitation of the corresponding generators. Such issues can be clarified by potential fields analysis with topographic mapping.

BIT-MAPPED IMAGING OF SEP

7

Color scaling for EP imaging Fig. 4 presents characteristic SEP traces recorded with earlobe reference. The P14 farfield is followed by the contralateral parietal N20 and P27 (Fig. 4C). At the frontal scalp, the P20 (concomitant with N20, Deiber et al. 1986) is followed by P22, N30 and P45 (Desmedt and Cheron 1980b, 1981b; Desmedt and Bourguet 1985). The parameters for SEP imaging were analyzed on SEPs at 3 chosen latencies (frozen maps): 20 msec to display N20-P20 fields, 25 msec for the prerolandic P22, and 33 msec for the frontal N30 and parietal P27 (Fig. 5). A first question is to optimize color steps for scalp topographies. With a scale of 0.4 ~tV (Fig. 5A-C), the N20, P20 (Fig. 5A) and P22 (Fig. 5B) were displayed with 3 or 4 color levels, while the larger frontal N30 looked somewhat confused with as m a n y as 10 color steps (Fig. 5C). When using a scale of 0.8 ffV, the N30 field structure was more clearly depicted with 5 hues (Fig. 5F) but the

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Fig. 4. Averaged SEPs to electric stimulation of left finger I-II in a normal male of 25 years. Right earlobe reference. Average of 4163 trials. A: left parietal site showing no early response after the P14 farfield, and a later small negativity diffusing from the front. B: right prerolandic site at 7 cm from midline (thick trace) superimposed on the left parietal trace. Components P20, P22 and P30 are seen after P14. C: right parietal site at 7 cm from midline (thick trace) superimposed on the left parietal trace and showing N20 and P27. In all figures, negativity produces an upward deflexion•

other components lost a lot of useful detail (Fig. 5 D - E ) . This was resolved, in the present example, by using 3 or 4 color steps of 0.4 #V followed by steps of 0.8 #V whereby the field details were adequately imaged for both small and large components (Fig. 5 G - I ) . It is wise not to exceed about 7 levels on each side since tonal transitions are more clearly discriminated when fewer. After polarity convention and color step size, one has to decide upon the sequence of hues to image voltage levels. Some publications have used dark colors for zero and small potentials and light colors (such as yellow or white) for maximum voltages. We think a more natural sequence is to use white or light gray for baseline on the view that no color implies no significant potential difference. Increasing voltages are then depicted by a shift from light to dark steps of blue for positive potentials, and by light to dark steps of green, yellow and then red for negative. Such a scale conforms to the spectral order since hues become warmer as potentials get more negative.

Non-cephalic versus earlobe reference for EP imaging Non-cephalic reference (NCR) recording minimizes cancellation of widespread components (Jewett and Williston 1971; Cracco and Cracco 1976; Desmedt and Cheron 1980a, 1981a) such as N18 that drives all scalp traces negative for nearly 20 msec (Fig. 6) (Desmedt and Cheron 1981b; Maugui6re et al. 1983b). Color imaging of N C R data displayed the focal SEP components on this negative-going baseline so that the frontal P20 (Fig. 7C) and prerolandic P22 (Fig. 7D) appeared as mere reductions from ambient N18 negativity (yellow-red) and only reached the first negative level (green) but not actual positivity (blue). The parietal P27 was also seen as a reduction from the N18 yellow-reds and its peak only reached zero level (gray) (Fig. 7E). The larger frontal P45 went into some positivity (Fig. 7F). Though confusing at first sight, such N C R maps were consistent with maps of the same SEPs recorded with earlobe reference (Fig. 5 G - I ) . Since N18 occurs at earlobes (Fig. 6A), using an earlobe reference subtracted N18 from the scalp traces whereby the N18 negative shift

8

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in NCR recordings since this depended on their voltage relative to that of the N18 in different subjects (Desmedt and Cheron 1981b). Fig. 8C shows actual positivity of P22 with NCR in spite of a sizeable N18. Average reference recording (Lehmann and Skrandies 1980) will be discussed elsewhere.

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Fig. 6. Same SEP recording session as in Fig. 4, but presented with a non-cephalic reference on right-hand dorsum. A: right earlobe showing P9-P14 farfields and N18. B: left parietal site ipsilateral to fingers stimulated: C: right prerolandic site (thick trace) superimposedon left parietal trace. D: right parietal site superimposed on left parietal trace. All traces are shifted upwards from zero (interrupted line) due to the widespread N18 generated in the brain-stem.

cancelled out (Fig. 4) or only left a low voltage negativity that remained constant during the early cortical SEP responses (Desmedt and Cheron 1981b). On the other hand, cortical SEP components were not recorded at the earlobes (Desmedt and Cheron 1980b). While NCR recording is necessary to depict subcortical "generators producing widespread farfields at the scalp, earlobe reference recording is best for easier discrimination of the negative and positive cortical SEP fields (Desmedt and Bourguet 1985; Deiber et al. 1986). In any case, we consider P22 or P27 as actual scalp positivities whether they actually did or did not cross the baseline to reach positive potentials

Critical electrodes in different montages Different electrode montages were analyzed by omitting chosen data from the standard 27-channel array so that the maps under comparison shared identical averaged data for electrodes they had in common. A 17-channel array (Fig. 9) based on the 10-20 EEG standard included the central (1.5 cm in front of Cz, see above), parietal and frontal coronal electrodes. This included the prerolandic P22 culmination charted by C4' (Fig. 5K) but actually missed the N20 (Fig. 5J) and P27 (Fig. 5L) foci that were no longer sampled by the additional coronal electrodes row between Cz and Pz used in the 27-channel array (Fig. 5G-I). Not much detail was lost in the large frontal P20 (Fig. 5J) or N30 (Fig. 5L) fields. The 14-channel array (Fig. 10) designed for SEPs by Desmedt and Bourguet (1985) used alternative coronal rows just in front and behind Cz, while dropping the central, frontal and parietal coronal rows of the 10-20 system. It disclosed the N20 (Fig. l l J ) and P27 (Fig. I l L ) culminations, but missed the P22 focus as the C4' electrode was lacking" (Fig: l l K ) . P20 and N30 were fairly displayed in spite of rather few electrodes over the front. Thus, electrodes charting rather extensive potential fields could be dropped without much loss of definition while other electrodes located near-field culminations were critical for adequate map resolution. When attempting to use electrodes sparingly while avoiding unacceptable loss of resolution, it is essential to prior identify critical recording sites for the EPs considered.

Fig. 5. Color imaging of SEPs to stimulation of left fingers I - I I in the same subject. 27-channel mapping at latencies of 20 msec (left column), 25 msec (second column) and 33 msec (fight column). Interpolation of averaged data at the 4 nearest electrodes with third power of distance. A - C : color scale with steps of 0.4/~V. D - F : color scale with steps of 0.8 ,ttV. G - L : color scale with steps of 0.4 and 0.8 p,V for 27-channel ( G - I ) or 17-channel (J-L) arrays.

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Fig. 8. Non-cephalic reference recording of SEPs to left median nerve stimulation in another normal male of 23 years. A: left parietal site showing N18 after the P9-Pll-P14 farfields. B: right parietal site (thick trace) superimposed on left parietal trace. C: right prerolandic site (thick trace) superimposed on left parietal trace. P20 and P22 crossed the zero baseline.

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.., Interpolation algorithms Our analysis of spatial interpolation algorithms identified as an important parameter the exponent chosen for distances (d b) from any pixel to the 4 nearest electrodes in computing electrode weights (Walter et al. 1984). Maps were computed from the same 27-channel bioelectric data with different exponents b from 1 to 12. For linear interpolation (b = 1) the peak loci of the N20 (Fig. 12A), P22 (Fig. 12B) or P27 (Fig. 12C) potential fields were. barely detectable while boundaries between color steps tended to be jagged. On the other hand, with

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b = 12 (Fig. 1 2 D - F ) color areas expanded into square or triangular shapes assuming the potential of the electrode on which they were centered. Among the 4 nearest neighbors considered in computing weights for each pixel, one was over-

Fig. 7. Color imaging of same data either with non-cephalic ( A - F ) or with right earlobe reference (G-I). 27-channel array. Interpolation of 4 nearest electrodes and third power of distance. Latencies are indicated about each frozen maps. G-I: drastic loss of detail when imaging the brain map with only 1000 (larger) pixels. J - L : checking amplifiers with - 10 ,~V (K) or + 10 t~V (L). The calibration presents at _+ 10 /W color steps of only 0.1 #V width to show consistency of amplification (better than 1%) for the 27 channels.

12

J.E. DESMEDT ET AL.

14 channels

Cz

..

......... Q

""°"°°°'° •

I. . . . . . . . . .

"f

..... 1

I

\

• -6 ~

t

t



"

-3

/ -

t

.

2 .

..,"~ .,.~

.=~=jl === Fig. 10. Location of electrodes in 14-channel montage. The circled pixel at right parietal region in B is used as example for different interpolations with 4 or 6 nearest electrodes and exponent b = 1 or 3 for distance in Table II.

whelming and the other 3 obviously had a negligible weight when exponent b exceeded about 5. Perusing different exponents led to the clear conclusion that the third power of distance (Fig. 12G-I) best disclosed peak foci and field contours that appeared plausible.

This empirical finding was in line with anticipations from calculations of potential fields generated by an equivalent dipole perpendicular to the cortical surface (Plonsey 1974; Nugaez 1981). Extracellular potentials fall off rather rapidly with distance so that a linear interpolation is rather unrealistic for computing electrode weights. From these calculations, the potential of a cortical dipole layer volume-conducted along the scalp (thus at right angle to dipole axis) roughly falls off in proportion to d-3 at distances that are large compared to dipole dimensions. The head curvature can be neglected since the head radius (about 8 cm) is'large compared to both dipole dimensions and interelectrode distances. These considerations support our suggestion based on experimental data that the interpolation algorithm should involve a cubic power of distance for scalp electrodes. The optimal choice for the number of nearest neighbors to be interpolated was analyzed. This parameter was quite sensitive for a 14-channel array where interelectrode distances were rather large (Fig. 10). When using the 6 nearest electrodes for pixel voltage computation, the linear interpolation (Fig. l l A - C ) gave a very poor imaging and the parietal P27 was virtually obliterated (C) while cubic interpolation (Fig. l I D - F ) achieved a much better resolution including for P27. When using the 4 nearest electrodes instead, the linear interpolation presented similar, though somewhat less severe, problems (Fig. l l G - I ) but cubic interpolation gave much better results (Fig. llJ-L). Table II documents these interpolation algorithms for an arbitrarily chosen pixel behind the parietal P27 focus (Fig. 10B). For computations based on the 6 nearest neighbors, frontal electrodes 5 and 6 contributed positive values for N20 and negative values for P27 thereby competing with actual readings at electrodes that were closer to the pixel considered. This contrary effect of adjacent scalp fields of opposite polarity was devastating with linear interpolation, but largely

Fig. 11. Color imaging of same data with fight earlobe reference and 14-channel array. Frozen map latencies at 20 msec (left column), 25 msec (middle) or 33 msec (right). Interpolation of either 6 ( A - F ) or 4 ( G - L ) nearest electrodes. The exponent for distance to pixel considered was b = 1 ( A - C and G - I ) or 3 ( D - F and J-L).

BIT-MAPPED I M A G I N G OF SEP

13

14

J.E. D E S M E D T ET AL

BIT-MAPPED IMAGING OF SEP controlled with cubic interpolation. While the 4-nearest-neighbor interpolation seemed an obvious choice for pixels located within the array, it can be argued on theory that a 3-nearest-neighbor interpolation would be better for pixels located at the margins of the array. This was tested but failed to disclose any decisive advantage provided a cubic interpolation algorithm was used (Fig. 12J-L). The span and voltage of color steps was identical for marginal pixels at the periphery of the maps whether a 4- (Fig. 1 2 G - I ) or a 3-nearest-neighbor interpolation (Fig. 12J-L) was used on the same SEP data. The third power of distance indeed appears as more critical for best interpolation in map creation.

15 Rolando fissure Prerolandi¢

R

/. : 1N20

Tangential oersus radial generators of early SEP components SEP latencies in Figs. 5, 11 and 12 were chosen to illustrate characteristic mapping problems, namely in the case of 2 roughly equivalent fields of opposite polarity (20 msec), of one circumscribed positive field P22 (25 msec) or of a strong extensive negativity adjacent to a focal positivity (33 msec). The data are also pertinent to current issues about dipole generators of early cortical SEPs. The contralateral N20 and P22 perirolandic responses have led to different hypotheses concerning their sources which have been located: first, in thalamocortical radiations (Celesia 1979; Chiappa et al. 1980); second, in a single tangential dipole in parietal cortex (Broughton 1969; Wood et al. 1985); and third, in combined tangential and radial dipoles in parietal and motor cortex (Desmedt and Cheron 1980b, 1981; Papakostopoulos and Crow 1980; Maccabee et al. 1983; Maugui~re et al. 1983a; Desmedt and Bourguet 1985). The present study deals with SEPs to skin and joint afferents from fingers that travel in the dorsal column pathway (Noel and Desmedt 1975) and do not consider muscle Ia afferents elicited by stimulation of mixed or motor nerves (Gandevia

t VPLo

3a VPLc

Fig. 13. Drawing of perirolandic SEP generators about 20 msec after contralateral median nerve or finger stimulation. Parasagittal section through Rolando fissure (drawn roughlyto scale) with cortical areas 2, 1, 3b, 3a and 4. Thalamocordcal inputs from VPLc to parietal cortex or from VPLo to motor area 4 are sketched. A tangential dipole in area 3b in the posterior bank of Rolando fissure (about 25 mm from the scalp surface) concomitantly generates the parietal N20 and the frontal P20 fields. A radial dipole in motor area 4 generates the prerolandic P22 field with distinct spatio-temporal features. (Modified from Fig. 8 of Desmedt and Bourguet 1985.)

et al. 1984). The results confirm the finding of Deiber et al. (1986) of diffuse frontal positivity P20 concomitant with the parietal N20 (Figs. 5G and 12G): this further documents as N20-P20 generator an equivalent dipole which is tangential to the scalp surface and located in parietal area 3b, at about 25 mm from scalp in the posterior bank of the Rolando fissure (Fig. 13). The neuron columns have indeed an antero-posterior orienta-

Fig. 12. Color imaging of same data with right earlobe reference and 27-channel array. Frozen map latencies at 20 msec (left column), 25 msec (middle) or 33 msec (right). Interpolation of 4 nearest electrodes (A-I) or 3 nearest electrodes (J-L) with different exponents for distance b =1 (A-C), 12 (D-F), or 3 (G-L).

16 tion in area 3b which is a major recipient of cutaneous inputs from the VPLc thalamic nucleus (Jones 1983). The oblique line of polarity reversal between the N20 and P20 fields (Fig. 12) roughly corresponds to Rolando fissure orientation (Deiber et al. 1986). Magnetic recordings assessed the tangential dipole depth and disproved the possible subcortical origin of N20 (Brenner et al. 1978; Okada et al. 1984). However, this is only part of the story. The hypothesis that a single tangential dipole accounted for the early perirolandic SEP (Broughton 1969; Allison et al. 1980; Wood et al. 1985) was challenged by Desmedt and Cheron (1980b, 1981b) who identified a prerolandic P22 positivity whose neural generators appeared to be distinct from those of the parietal N20 because of a significant difference in latencies. Desmedt and Bourguet (1985) disclosed by topographic imaging the concentric positive isopotentials with no adjacent negativity of the prerolandic P22 field (Figs. 5H and 12, middle column) thereby documenting an equivalent cortical dipole with radial orientation with respect to the scalp. Their Fig. 8 tentatively involved radial equivalent dipoles over both motor and parietal cortices in addition to the tangential dipole. These dipoles were presented as a simplified model of the complex underlying neuronal phenomena which presumably involve several subareas during this slice of time. New evidence about the extensive P20 field representing the frontal counterpart of the parietal N20 raised the question whether P20 was indeed to be considered distinct from the P22 suggested by Desmedt and Cheron (1980b, 1981b). If not, the Broughton (1969) hypothesis would appear substantiated. However, the question cannot be resolved by mere inspection of SEP traces. For example, the longer latency of P22 with respect to that of N20 (Desmedt and Cheron 1981b) was only arguable if P22 could be properly differentiated from P20. Topographic imaging provided critical evidence at this point by documenting the distinct spatial features to tell P22 apart from P20 (Figs. 5H and 12). Deiber et al. (1986) further showed that the P22 focus (but not the N20-P20) shifted more medially over the scalp when the

J.E. DESMEDTET AL. stimulus was moved from contralateral thumb to fifth finger. Magnetic recordings are blind to radial sources (Brenner et al. 1978; Okada et al. 1984) and offered no cue about the radial dipole proposed by Desmedt and Cheron (1980b, 1981b). The most critical evidence for a location in motor area 4 of the radial P22 equivalent dipole was provided by studies of patients with a focal parietal vascular lesion, contralateral hemianesthesia without hemiplegia, and dissociated loss of parietal N20 with preservation of prerolandic P22 (Mauguirre et al. 1983a). These results documented in man that separate short-latency thalamocortical somatosensory inputs reached the motor cortex. There is anatomical evidence in the monkey that exteroceptive afferents relay in thalamic VPLo nuclei with fast direct projection to the motor area 4 (Tracey et al. 1980; Jones 1983). Motor cortex neurons respond with short latency to skin and joint afferents from contralateral hand (Rosrn and Asanuma 1972; Wong et al. 1978; Lemon and Vanderburg 1979; Asanuma et al. 1980; Lemon 1981; Tanji and Wise 1981). Although SEP components may be different in the monkey, median nerve stimulation elicited distinct neuronal responses in the posterior bank (N10-P10) and anterior bank (P13) of the Rolando sulcus (Arezzo et al. 1981). Thus, a single tangential dipole cannot account for the recorded early SEP response and it is necessary to add another dipole in motor cortex. The drawing proposed by Desmedt and Bourguet (1985, Fig. 8) tentatively included 2 radial dipoles in addition to the tangential dipole. This is now amended by removing the radial parietal dipole for which no specific evidence has been provided at this stage (Fig. 13). This current simplest model for the generation of early cortical SEP components thus involves: (1) a tangential equivalent dipole in area 3b (posterior flank of Rolando fissure) which is activated by thalamocortical afferents from VPLc and generates the parietal N20 and frontal P20 scalp fields concomitantly; (2) with a delay of 1-2 msec, a radial equivalent dipole in motor area 4 which is activated by thalamocortical afferents from VPLo and generates the prerolandic P22 scalp field.

BIT-MAPPED IMAGING OF SEP

Conclusion Bit-mapped imaging of EPs accurately displays rapidly evolving brain potential fields over distinct scalp locations with adequate time resolution. Such evidence is invaluable for analyzing the sequential activation of the distinct neural generators that involve different cortical areas over time. It would be impossible to mentally conceive such detailed spatio-temporal features by mere inspection of the EP wave forms that actually served to compute the bit-mapped images. SEP components with their sharp rise times and distinct scalp locations actually represent a more difficult challenge than, say, visual EPs. Updated imaging involves a coherent set of methodological requirements, namely for system bandpass, accuracy of averaging for the different channels and interference control. About 25 channels with critical positioning of electrodes can chart both hemispheres and scalp sites where EP components culminate. Each map should include about 4000 pixels. Pixel values are best computed by interpolation between 4-nearest electrodes with third power exponent of the distances. Linear interpolation is much less satisfactory and is not in line with volume conductor theory. For color imaging, it is proposed to ascribe warm reds to negativities and cold blues to positivities. About 7 color steps of different hue or saturation are used for either positive or negative scales. The pixels of each color step should involve hue, saturation and dot pattern designs for optimum visual identification. Color step size can be modulated for imaging in detail both smaller and larger EP components. The analysis of early cortical SEP components with bit-mapped imaging critically documents the spatial features that tell apart the extensive P20 (which is the frontal counterpart of the parietal N20) from the prerolandic P22. Somatosensory input from fingers activates two distinct sets of cortical neurons located in the posterior flank of the Rolando fissure and in the motor area 4 respectively through separate thalamocortical pathways. The first set of neurons centered in parietal area 3b generates a tangential equivalent dipole that concomitantly produces the N20 field in the parietal scalp and the P20 field over the

17 front. The second set of neurons in motor cortex generates a radial equivalent dipole that produces the prerolandic P22 response. Magnetic recordings only display the tangential dipole whereas topographic mapping of somatosensory potentials discloses both tangential and radial generators.

R~sum~

Comment r$aliser l'imagerie digitale des potentiels $voqu$s chez l'homme L'imagerie digitale des champs de potentiels crrrbraux 6voqurs par stimulation sensorielle chez l'homme met en 6vidence des faits qui ne sont pas 6vidents lors de l'observation des tracrs multicanaux. On considrre en d&ail les problrmes de mrthodes pour les potentiels somesthrsiques qui comportent beaucoup de composantes rapides /~ localisations distinctes. Un systrme d'imagerie efficace n~cessite un nombre suffisant d'rlectrodes en des endroits critiques du cuir chevelu, une bande passante rrsolvant les composantes rapides, des logiciels et des 6chelles de couleurs approprirs. Les points critiques de ces mrthodes ont 6t6 analysrs et discut,s.

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