Effective connectivity maps in the swine somatosensory cortex estimated from electrocorticography and validated with intracortical local field potential measurements

Abstract

Macroscopic techniques are increasingly being used to estimate functional connectivity in the brain, which provides valuable information about brain networks. In any such endeavors it is important to understand capabilities and limitations of each technique through direct validation, which is often lacking. This study evaluated a multiple dipole source analysis technique based on electrocorticography (ECOG) data in estimating effective connectivity maps and validated the technique with intracortical local field potential (LFP) recordings. The study was carried out in an animal model (swine) with a large brain to avoid complications caused by spreading of the volume current. The evaluation was carried out for the cortical projections from the trigeminal nerve and corticocortical connectivity from the first rostrum area (R1) in the primary somatosensory cortex. Stimulation of the snout and layer IV of the R1 did not activate all projection areas in each animal, although whenever an area was activated in a given animal, its location was consistent with the intracortical LFP. The two types of connectivity maps based on ECOG analysis were consistent with each other and also with those estimated from the intracortical LFP, although there were small discrepancies. The discrepancies in mean latency based on ECOG and LFP were all very small and nonsignificant: snout stimulation, -1.1-2.0 msec (contralateral hemisphere) and 3.9-8.5 msec (ipsilateral hemisphere); R1 stimulation, -1.4-2.2 msec for the ipsilateral and 0.6-1.4 msec for the contralateral hemisphere. Dipole source analysis based on ECOG appears to be quite useful for estimating effective connectivity maps in the brain.

FIG. 1.

Cerebral cortex of juvenile swine (example animal 0670). Stimulating (star) and recording (dots, n=59) electrode positions. Outline of the cerebral cortex reconstructed from a photograph. SI includes R1 and R2—nomenclature from Craner and Ray (1991a). Snout represented contralaterally and somatotopically around the coronal gyrus and the surrounding sulci and sulcus naris (n). R2 is in the sigmoid gyrus. SII is lateral to the coronal gyrus of R1 within and along the ss. SI, primary somatosensory; SII, secondary somatosensory; ss, suprasylvian sulcus.

FIG. 2.

Epipial ECOG signals elicited by left snout stimulation and cortical sources estimated from the ECOG data. Electric stimuli to the left medial snout. ECOGs were simultaneously measured with 106 electrodes placed on the epipial cortical surface. (A) Superimposed ECOG waveforms for the 106 channels. (B) Surface Laplacian map 60 msec post-stimulus. (C) Dipole source analysis. Location and orientation of each ECD shown by a bar. Each dipole is located in the midpoint, and directed toward the red side. Left: Locations of five sources are superimposed on the horizontal and coronal views of the electrode array and an outline of the exposed cortex determined with Polhemus FASTRAK. Right: Waveforms of the five sources. ECD, equivalent current dipole; ECOG, electrocorticography.

FIG. 3.

Epipial ECOG signals elicited by direct electric stimulation of the layer IV of the right R1 cortex. Stimulation point, red star in (B) and (C). (A) Superimposed ECOG waveforms for the 106 channels. (B) Surface Laplacian maps at 60 msec post-stimulus. (C) ECD position and orientation (left) and source waveforms (right). Left R2 source seen in (B) was not identified by the dipole analysis.

FIG. 4.

Intracortical LFPs elicited by the snout stimulation (location shown by red star in animal 0696) in various regions of the somatosensory cortex. Stimulation elicited responses in left SII (1), left R1 (2), right R2 (3), right SII (4), and right R1 (5). These potentials showed focal activation with clear polarity reversals across the cortical layers in each area. LFP, local field potential.

FIG. 5.

Projection maps for the trigeminal nerve (snout). (A) Group summary of the connectivity map. Stimulation activated the contralateral right R1, R2, and SII, and ipsilateral left R2 and SII. (B) Top row: individual data of the four animals studied. Bottom row: maps of corticocortical connectivity from right R1 (at the location of maximum projection from the same snout position) in the same animals. Although the number of activated sites was variable across the animals, any given projection area when activated was very similar between the snout and R1 stimulation conditions.

FIG. 6.

Intracortical LFP elicited by stimulation of the layer IV of the right R1 (shown by red star) in various regions of the somatosensory cortex. LFPs were recorded at the positions indicated by dots, along the cortical lamina at the depths from 0.0 to 2.0 mm with 0.5 mm at each position. LFP waveforms are shown at the peak location in each area. (A) Responses in the hemisphere ipsilateral to stimulation. (B) Responses in the hemisphere contralateral to stimulation. Note polarity reversal along the cortical depth at each projection area.

FIG. 7.

Forward corticocortical connectivity map originating from right R1. (A) Connectivity map for the group. Electric stimulation in right R1 cortex (star) activated ipsilateral R2 and SII, and contralateral R1 and SII. (B) Connectivity maps for individual animals (n=9). Star shows the stimulation site for each animal. Open circles indicate activation sites with vertically oriented cortical currents directed from the deep cortical layers toward the cortical surface. Filled circles with a stick indicate the activation site with horizontally directed currents, probably located in the sulcus. Although not all four areas were activated in any given animal, the active site closely matched the group data when a given area was activated.

FIG. 8.

Summary of the cortical connectivity maps in the swine somatosensory cortex. Thick arrows indicate hypothesized direct forward connections. Dotted lines indicate probable indirect connections. Mean onset latency is shown for each pathway. Right R1 area provides direct forward connections to right R2 and SII and left R1 and SII, but not R2. The homotopic areas of left and right R1 appear to be bidirectionally connected. Snout projects to right R1, R2, and SII and left R2 and SII, but not left R1. The onset latencies of evoked responses are very similar based on ECOG (green) and intracortical LFP (black).