Contributions of principal neocortical neurons to magnetoencephalography and electroencephalography signals

Abstract

A realistically shaped three-dimensional single-neuron model was constructed for each of four principal cell types in the neocortex in order to infer their contributions to magnetoencephalography (MEG) and electroencephalography (EEG) signals. For each cell, the soma was stimulated and the resulting intracellular current was used to compute the current dipole Q for the whole cell or separately for the apical and basal dendrites. The magnitude of Q is proportional to the magnetic field and electrical potential far from the neuron. A train of spikes and depolarization shift in an intracellular burst discharge were seen as spikes and an envelope in Q for the layer V and layer II/III pyramidal cells. The stellate cells lacked the envelope. As expected, the pyramidal cells produced a stronger Q than the stellate cells. The spikes produced by the layer V pyramidal cells (n = 4) varied between -0.78 and 2.97 pA m with the majority of the cells showing a current toward the pia (defined as positive). The basal dendrites, however, produced considerable spike currents. The magnitude and direction of dipole moment are in agreement with the distribution of the dendrites. The spikes in Q for the layer V pyramidal cells were produced by the transient sodium conductance and potassium conductance of delayed rectifier type; the conductances distributed along the dendrites were capable of generating spike propagation, which was seen in Q as the tail of a triphasic wave lasting several milliseconds. The envelope was similar in magnitude (-0.41 to -0.90 pA m) across the four layer V pyramidal cells. The spike and envelope for the layer II/III pyramidal cell were 0.47 and -0.29 pA m, respectively; these values agreed well with empirical and theoretical estimates for guinea pig CA3 pyramidal cells. Spikes were stronger for the layer IV spiny stellate (0.27 pA m) than the layer III aspiny stellate cell (0.06 pA m) along their best orientations. The spikes may thus be stronger than has been previously thought. The Q for a population of stellate cells may be weaker than a linear sum of their individual Q values due to their variable dendritic geometry. The burst discharge by pyramidal cells may be detectable with MEG and EEG when 10 000-50 000 cells are synchronously active.

Figure 1. Reconstructed shapes, firing patterns and intracellular current dipole moments of neocortical neurons

Reconstructed neuron models from cat visual cortex (A–C) and rat somatosensory cortex (D); shapes of cells (row 1), evoked firing patterns (row 2) and current dipole moments (row 3) for a layer V pyramidal cell (A), layer II/III pyramidal cell (B), layer IV spiny stellate cell (C), and layer III aspiny cell (D). Geometries of the cells were taken from the 1996 Mainen model. A constant current was injected into the soma (200 pA, 100 pA, 70 pA, 50 pA for A–D, respectively). Positive polarity indicates currents directed from a deep layer to the surface for the pyramidal cells. Unit dipoles that maximize the dot products were used for the layer IV spiny and the layer III aspiny cells. Positive polarity indicates currents directed from the bottom to the top of the figure for layer IV spiny stellate cell and layer III aspiny cell.

Figure 2. Reconstructed shapes, firing patterns and intracellular current dipole moments of layer V neocortical pyramidal cells

Row 1: cellular geometry of the three layer V pyramidal cells taken from Stuart & Spruston (1998). Row 2: intracellular potentials produced by current injection (200 pA) into the soma. Row 3: current dipole moment Q for the layer V pyramidal cells. Passive and active properties were taken from the 1996 Mainen model. Positive polarity indicates currents directed from a deep layer to the surface.

Figure 3. Contribution of dendrites to current dipole moments in layer V pyramidal cells

Row 1: intracellular potential from the four layer V pyramidal cells. Row 2: current dipole moment Q of a whole cell (dotted curve) and of the apical dendritic segments (continuous curves) for each cell. Row 3: current dipole moment Q of a whole cell (dotted curve) and of the basal dendritic segments (continuous curves) for each cell. A, layer V pyramidal cell from the 1996 Mainen model. B–D, three layer V pyramidal cells based on morphological data from Stuart & Spruston (1998).

Figure 4. Contribution of sodium conductance g_Na and potassium conductance of delayed rectifier g_K(DR) in a layer V pyramidal neuron with varying active channel properties

Top four rows: intracellular potentials at basal dendritic terminal (row 1), soma (row 2), first branching point of the apical dendrite (row 3), and apical dendritic terminal (row 4). Bottom three rows: current dipole moments of whole cell (row 5), apical dendritic segment (row 6) and basal dendritic segment (row 7). A, cell with g_Na and g_K(DR) only in the soma with passive basal and apical dendrites. B, cell with g_Na and g_K(DR) distributed throughout the basal and proximal apical dendrites up to the first branching point. C, same as cell in b except g_Na and g_K(DR) were distributed uniformly throughout the dendrites. g_Na = 40 pS μm⁻² for cells in A–C. D, same as cell in c except g_Na = 100 pS μm⁻².