1. A quantitative 2-[14C]deoxy-D-glucose (2DG) autoradiographic study was undertaken to determine the functional (metabolic) organization of an individual column in the first somatosensory cortex (SI) of the awake restrained rat. Manual or mechanically controlled brush stroking of a single vibrissa (typically C3) was used in order to evoke neural activity and increase glucose utilization in a single cortical barrel in lamina IV and in adjacent supra- and infragranular layers in register with the single cortical barrel labeling in lamina IV. 2. The single activated vibrissal column was found to extend from layer I to the superficial half of layer VI of the contralateral SI cortex and was fusiform in shape, being of largest diameter (650-micron) in layer IV and smallest diameter (200 micron) in layer VI. 3. This single metabolic column was not uniform in its density of labeling. The greatest local cerebral metabolic rate of glucose (LCMRG) was found in layer IV (170 mumol.100 g-1.min-1), layers II-III, and V had, on the average, similar LCMRG values (115 mumol.100 g-1.min-1), which decreased with distance from layer IV. 4. The functional (metabolic) columnar activity center situated in layer IV corresponded in size to the appropriate anatomical barrel as determined from thionin-stained sections. Increased metabolic activity was not strictly confined to the candle-pin-shaped column but extended tangentially as radiating fingerlike projections toward the neighboring barrels. 5. In cortical layers other than IV, the metabolic column was less prominently labeled, and the metabolic activity also branched in the tangential plane. The labeling pattern profile in upper layers was characterized by numerous lateral spreading fingerlike projections of increased glucose metabolism. 6. Neonatal follicle lesions sparing only C3 vibrissa caused a great increase (125%) in cortical territory driven by the spared whisker with a concomitant loss of columnar shape and decrease in intensity of metabolic activity in response to its stimulation. 7. Similar lesions in adult rats produced a significant increase (40%) in dimensions of the spared C3 cortical column, which was, however, smaller than that produced after neonatal lesions. The metabolic activation of layer Vb in the spared C3 column was increased (17%) compared with that of the control column.(ABSTRACT TRUNCATED AT 400 WORDS)