Epidural mapping of flash-VEP in awake monkeys revealed a reliable, short latency negativity, N25 (onset: 18-22 msec; peak: 23-27 msec; duration: 15-20 msec), with a broad frontal surface distribution (frontolateral maximum). N25 was dissociable from the electroretinogram (ERG), from cortical VEP and from the high frequency oscillations (wavelets) coextensive with the ERG and with cortical VEP. Depth recordings traced N25 from its surface maximum down to the lateral geniculate nucleus (LGN). Concomitant VEP, current source density (CSD) and multiunit activity (MUA) profiles obtained with multicontact electrodes showed that the peak and later portion of N25 arise primarily from current sinks (associated with MUA increases) that reflect transmembrane current flow attending depolarization of cells in lamina 6, the uppermost lamina, but may also receive contributions from the more ventral LGN laminae. The initial portion of N25 arises from similar processes near the lamina 3/2 border. Wavelets, in contrast, are prominent in VEP, CSD and MUA within LGN, but attenuate rapidly above LGN. LGN laminar and cellular morphology predict volume conduction of N25 over a wide arc lateral and anterior to LGN and roughly horizontal isopotential planes medial and posterior to LGN. Recordings on the brain surface, within LGN, and in the regions surrounding LGN are consistent with these predictions. Possible contributions from other structures and how these results fit with data obtained in humans are considered.