Effect of Transient Cerebral Ischemia on Metabolic Activation of a Somatosensory Circuit

Abstract

The effects of transient ischemia on the metabolic responsiveness of a well-defined brain circuit were investigated with [¹⁴C]2-deoxyglucose autoradiography. Rats underwent 30 min of severe forebrain ischemia followed by postischemic recirculation periods of 1, 2, 3, 5, and 10 days. At these times, unilateral whisker stimulation was carried out, resulting in the metabolic activation of the whisker barrel circuit. An altered pattern of glucose utilization within both stimulated and nonstimulated circuit relay stations was observed at 1, 2, and 3 days following ischemia. At 1 day, stimulus-evoked increases in metabolic activity were severely depressed within both the ventrobasal thalamus and layer IV of the cortical barrel field region. Baseline metabolic rate within nonstimulated relay areas was also severely depressed at this time. At postischemic days 2 and 3, moderate levels of increased glucose utilization were apparent overlying cortical layer IV and the superficial half of layer VI, while layers I, II, III, and V appeared less responsive to metabolic activation. By day 5, whisker stimulation resulted in normal levels of increased glucose utilization within the activated ventrobasal thalamus and layer IV of the cortical barrel field region. Glucose utilization within nonactivated relay stations, depressed at earlier time periods, had also returned to control levels by day 5. At both 5 and 10 days, an altered laminar pattern of elevated glucose utilization was apparent within the activated barrel field region, with local CMR_glu being depressed in layer V compared with control values. These results demonstrate that periods of transient ischemia produce both reversible and longer-lasting effects on the ability of the CNS to respond to peripheral activation. Functional restitution occurs slowly over a period of days following ischemia and appears to be related to the postischemic baseline level of metabolic rate. Finally, the abnormal laminar pattern of cortical activation apparent at postischemic day 10 may suggest dysfunction of intracortical circuits, a result that might be expected to alter the processing of sensory information.