Js. Mccasland et Ls. Hibbard, GABAERGIC NEURONS IN BARREL CORTEX SHOW STRONG, WHISKER-DEPENDENT METABOLIC-ACTIVATION DURING NORMAL BEHAVIOR, The Journal of neuroscience, 17(14), 1997, pp. 5509-5527
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.