ORGANIZATION OF INHIBITION IN THE RAT OLFACTORY-BULB EXTERNAL PLEXIFORM LAYER

1. Intracellular recordings were made from the output neurons (mitral and tufted cells) of the rat olfactory bulb during electrical orthodro mic stimulation of the olfactory nerve layer (ONL) and antidromic stim ulation of the lateral olfactory tract and posterior piriform cortex ( pPC) to test for physiological differences among the neuron types. Man y of these neurons were identified by intracellular injections of bioc ytin, and others were identified by their pattern of antidromic activa tion. 2. Both marked and unmarked mitral cells showed large inhibitory postsynaptic potentials (IPSPs) in response to antidromic stimulation of the pPC, whereas tufted cells exhibited small IPSPs in response to pPC stimulation. Tufted cells, however, showed large IPSPs in respons e to ONL stimulation. In many cases, these tufted cell responses to ON L stimulation were larger than the mitral cell responses. The marked s uperficial tufted cells, those with basal dendrites in the superficial sublayer of the external plexiform layer (EPL), had the smallest IPSP s in response to pPC stimulation. These data support anatomic observat ions suggesting that the granule cell populations responsible for the IPSPs may be different for mitral and for superficial tufted cells. 3. The different types of output cells also showed differences in their responses to orthodromic stimulation. Type I mitral cells, which have basal dendrites confined to the deep sublayer of the EPL, were signifi cantly less excitable by ONL stimulation than were the type II mitral cells, which have basal dendrites distributed within the intermediate sublayer of the EPL. Half of the type I mitral cells could not be exci ted at all by ONL stimulation. Superficial tufted cells showed even gr eater orthodromic excitability than type II mitral cells, usually resp onding to ONL stimulation with two or more spikes. 4. The ionic basis of the IPSPs in the superficial tufted cells appeared similar to those described for mitral cells. These IPSPs could be reversed by chloride injection and were associated with increased membrane conductance. 5. For both mitral and tufted cells, the number of ONL electrodes evokin g IPSPs was greater than the number evoking spikes. These data suggest a kind of center-surround organization of inputs to these cells from the ONL, although this does not yet imply that the sensory receptive f ield of these output cells has a center-surround organization. 6. In c onclusion, the properties of rat olfactory bulb output cells correlate with the sublayers of the EPL in which their basal dendrites lie. Tho se with basal dendrites in the superficial sublayer (superficial tufte d cells) are most easily activated by ONL stimulation, those with basa l dendrites in the deep sublayer (type I mitral cells) are least easil y activated, and those with basal dendrites in the intermediate layer (type II mitral cells, intermediate tufted cells, and internal tufted cells) are intermediate in ease of activation through this route. The cells with basal dendrites in the superficial sublayer receive very li ttle inhibition from stimulation of the pPC, which strongly inhibits c ells of the other two sublayers by activating the granule cells with s pines in the deeper sublayers. The fact that both mitral and superfici al tufted cells produce large chloride-dependent IPSPs in response to different inputs suggests that the different electrophysiological prop erties observed here may be due to the connectivity of the cells rathe r than to any differences in the IPSP mechanisms.