Apparent discrepancy between single-unit activity and [14C]deoxyglucose labeling in optic tectum of the rattlesnake

Abstract

Autoradiographic analysis of [1-14C]2-deoxy-D-glucose-6-phosphate ([14C]2-DG-P) accumulation in the rattlesnake brain stem and optic tectum was used in an effort to map infrared and visual neuronal pathways. Visual stimulation with a standard stimulus (a heat lamp) resulted in dense labeling of the superficial layers of the optic tectum. Infrared stimulation with the same standard stimulus resulted in labeling at the first synaptic relay, the lateral descending nucleus of the trigeminal tract (LDN-V), but not at higher levels, including the optic tectum. Systematic comparison of electrophysiological properties of tectal neurons was performed using the standard stimulus. Responses of infrared units in one hemitectum and visual units in the other, elicited by the same stimulus used in the [14C]2-DG-P experiments, were analyzed. There were no clear differences in the number, maximal density, spread, or rates of accommodation of visual units and infrared units, although the locus of maximal density was more superficial for visual units. In general, infrared units generated a greater number of action potentials than did visual units. All infrared units responded only to onset of the stimulus but they varied greatly in their ability to maintain discharge for the full duration of the stimulus. Most visual units exhibited on-, off-, or on-off responses. Four units showed only inhibition of spontaneous activity during the visual stimulation. There were significant differences in the evoked responses elicited by visual and infrared stimulation in response to the standard stimulus. Infrared stimuli generated single, large, triphasic on-responses, whereas visual stimulation generated complex multiphasic and long-lasting on- and off-responses. The major infrared on peak reached maximal amplitude at greater depths and was larger than the major visual on peak. Amplitude of the infrared peak fell off more rapidly with distance from the locus of its maximum than did amplitude of the visual peak. These observations are consistent with the view that infrared stimulation is effective in discharging neurons but is not associated with intense synaptic excitation. In contrast, visual stimulation apparently does produce intense synaptic activity, as suggested by the duration, complexity, and spread of the visual evoked response. Failure of this synaptic activity to produce more spikes in visual units probably reflects either depolarizing spike inactivation or the admixture of excitatory and inhibitory actions. Our observations suggest that 2-deoxy-D-glucose uptake is not necessarily correlated with the degree of action potential activation of specific neuronal pathways. The amount of [14C]2-DG-P labeling may reflect the metabolic requirements for support of synaptic depolarization as well as that supporting action potentials.