For about six decades, primary current sources of the electroencephalogram (EEG) have been assumed dipolar in nature. In this study, we used electrophysiological recordings from anesthetized Wistar rats undergoing repeated whisker deflections to revise the biophysical foundations of the EEG dipolar model. In a first experiment, we performed threedimensional recordings of extracellular potentials from a large portion of the barrel field to estimate intracortical multipolar moments generated either by single spiking neurons (i.e., pyramidal cells, PC; spiny stellate cells, SS) or by populations of them while experiencing synchronized postsynaptic potentials. As expected, backpropagating spikes along PC dendrites caused dipolar field components larger in the direction perpendicular to the cortical surface (49.7 Ϯ 22.0 nA·mm). In agreement with the fact that SS cells have "close-field" configurations, their dipolar moment at any direction was negligible. Surprisingly, monopolar field components were detectable both at the level of single units (i.e., Ϫ11.7 Ϯ 3.4 nA for PC) and at the mesoscopic level of mixed neuronal populations receiving extended synaptic inputs within either a cortical column (Ϫ0.44 Ϯ 0.20 A) or a 2.5-m 3 -voxel volume (Ϫ3.32 Ϯ 1.20 A). To evaluate the relationship between the macroscopically defined EEG equivalent dipole and the mesoscopic intracortical multipolar moments, we performed concurrent recordings of high-resolution skull EEG and laminar local field potentials. From this second experiment, we estimated the time-varying EEG equivalent dipole for the entire barrel field using either a multiple dipole fitting or a distributed type of EEG inverse solution. We demonstrated that mesoscopic multipolar components are altogether absorbed by any equivalent dipole in both types of inverse solutions. We conclude that the primary current sources of the EEG in the neocortex of rodents are not precisely represented by a single equivalent dipole and that the existence of monopolar components must be also considered at the mesoscopic level.electroencephalogram; neocortex; multipolar current sources; inverse problem THE DIPOLAR MODEL, used by generations of neuroscientists to represent the current sources of the electroencephalogram (EEG) in humans (Niedermeyer and Lopes da Silva 1987; Nunez and Srinivansan 2006;Plonsey 1969;Walter and Walter 1949), has roots in early interpretations by Adrian and Matthews (1934) about the origin of the Berger rhythm (i.e., the alpha rhythm). These authors suggested that the cortical electric potentials formerly observed by Berger (1929) were caused by electrical sources close to the brain surface with a polarity inversion in the axis perpendicular to it. The existence of dipole-like field distributions with axes parallel to the cortical surface was later suggested by Beevers (1944), with confirmations for the kappa rhythm (Kennedy et al. 1948) and the epileptic focal seizures (Gumnit and Takahashi 1965). This model, which eventually gained popularity in many other eme...