Maturation of the neuronal metabolic response to vibrissa stimulation in the developing whisker-to-barrel pathway of the mouse

Abstract

We examined functional maturation in the mouse whisker-to-barrel pathway from P2 (P0 is the day of birth) to adulthood using the autoradiographic deoxyglucose (DG) method. After intraperitoneal DG injection, left whiskers C1-3 and E1 were stimulated. Sections were cut transversely through the brainstem, and coronally or tangentially through the parietal cortex. After autoradiography, the sections were stained for Nissl or for cytochrome oxidase (CO) activity. In subnuclei caudalis and interpolaris of the spinal trigeminal nucleus ipsilateral to stimulation, DG uptake evoked by the deflection of whiskers C1-3 was present at P2; in subnucleus oralis, nucleus principalis and the contralateral nucleus ventrobasalis of the thalamus, at P4; and in the contralateral barrel cortex, at P7. The first stimulus-dependent DG uptake appeared a few days after the appearance of whisker-related patterns seen in the CO- or Nissl-stained sections. In subnuclei caudalis and interpolaris, areas of stimulus-dependent DG uptake were initially larger than the CO segments representing the stimulated whiskers. Later, areas of stimulus-dependent DG uptake and CO segments matched well. DG uptake evoked by the stimulation of whisker E1 appeared 2-3 days later than that evoked by stimulation of whiskers C1-3. In nucleus principalis, one large area of stimulus-dependent DG uptake covered the representations of the caudal whiskers of all five rows--an observation made at all ages studied. In thalamus, stimulus-dependent DG uptake was found laterally in nucleus ventrobasalis. In barrel cortex, at P7, stimulus-dependent DG uptake was restricted to layers III and IV, but covered more barrels than whiskers stimulated. At P9, a second spot of high DG uptake was seen in deep layer V in register with that in layers III and IV. From P10 onwards, stimulus-dependent DG uptake stretched from layer II to layer VI, and in layer IV, in which it was highest, it was restricted to the barrels C1-3 and E1. In all stations, stimulus-dependent DG uptake decreased in magnitude after P10. While the onset of stimulus-dependent DG uptake is the result of the establishment of functional projections up to that station, the subsequent changes in size of the responding areas may well be due to the partial elimination of terminals, the maturation of local inhibitory circuits, and/or the development of cortical projections to the nuclei of termination and to the thalamic relay.