GABAERGIC NEURONS IN BARREL CORTEX SHOW STRONG, WHISKER-DEPENDENT METABOLIC-ACTIVATION DURING NORMAL BEHAVIOR

Electrophysiological data from the rodent whisker/barrel cortex indica te that GABAergic, presumed inhibitory, neurons respond more vigorousl y to stimulation than glutamatergic, presumed excitatory, cells. Howev er, these data represent very small neuronal samples in restrained, an esthetized, or narcotized animals or in cortical slices. Histochemical data from primate visual cortex, stained for the mitochondrial enzyme cytochrome oxidase (CO) and for GABA, show that GABAergic neurons are more highly reactive for CO than glutamatergic cells, indicating that inhibitory neurons are chronically more active than excitatory neuron s but leaving doubt about the short-term stimulus dependence of this a ctivation. Taken together, these results suggest that highly active in hibitory neurons powerfully influence relatively inactive excitatory c ells but do not demonstrate directly the relative activities of excita tory and inhibitory neurons in the cortex during normal behavior. We u sed a novel double-labeling technique to approach the issue of excitat ory and inhibitory neuronal activation during behavior. Our technique combines high-resolution 2-deoxyglucose (2DG), immunohistochemical sta ining for neurotransmitter-specific antibodies, and automated image an alysis to collect the data. We find that putative inhibitory neurons i n barrel cortex of behaving animals are, on average, much more heavily 2DG-labeled than presumed excitatory cells, a pattern not seen in ani mals anesthetized at the time of 2DG injection. This metabolic activat ion is dependent specifically on sensory inputs from the whiskers, bec ause acute trimming of most whiskers greatly reduces 2DG labeling in b oth cell classes in columns corresponding to trimmed whiskers. Our res ults provide confirmation of the active GABAergic cell hypothesis sugg ested by CO and single-unit data. We conclude that strong activation o f inhibitory cortical neurons must confer selective advantages that co mpensate for its inherent energy inefficiency.