INNERVATION OF BURST FIRING SPINY INTERNEURONS BY PYRAMIDAL CELLS IN DEEP LAYERS OF RAT SOMATOMOTOR CORTEX - PAIRED INTRACELLULAR-RECORDINGS WITH BIOCYTIN FILLING

Intracellular recordings were obtained from a class of neuron defined electrophysiologically as burst firing interneurons in layers V and VI in slices of adult rat somatomotor cortex. Four of these cells were r ecovered histologically. These four cells had resting membrane potenti als between -68 and - 80 mV, a mean input resistance of 77 +/- 16.2 Mn (measured from the voltage deflection produced by a 100 ms, 0.5 nA hy perpolarizing pulse delivered from a membrane potential of - 80 mV) an d responded to injections of depolarizing current from membrane potent ials negative of - 70 to - 75 mV with an initial burst of action poten tials followed by a complex afterhyperpolarization. In response to inj ection of larger (0.5-1.5 nA) hyperpolarizing current pulses from memb rane potentials between - 60 and - 70 mV, 15 of 20 burst firing cells (three of four recovered histologically) that were tested displayed de layed inward rectification, and in all 20 cells of this type, response s to large negative current pulses were followed by a rebound depolari zation that could initiate action potentials. Filling of four of these cells with biocytin and subsequent histological processing revealed t hat they were bitufted with sparsely to medium spiny dendrites and ext ensive local axon ramifications. These neurons are similar to low thre shold spiking cells [Kawaguchi (1993) J. Neurophysiol. 69, 416-431]. U ltrastructural examination of the axons of three cells revealed that o f 53 labelled terminals studied, the majority formed synaptic contacts with dendritic shafts. Filling neurons with biocytin during paired in tracellular recordings resulted in three well labelled interneurons, e ach of which was postsynaptic to a simultaneously recorded pyramidal n euron. In these pairs both cells were identified, but the presynaptic axon was poorly labelled in one. In one of the two pairs in which the pre- and postsynaptic neurons were fully recovered, light microscopic assessment indicated that the axon of the presynaptic pyramid formed 1 2 close appositions with dendrites of the postsynaptic interneuron. Si x of these appositions were examined at the electron microscopic level and were identified as possible synaptic contacts. In the other pair three of six close appositions observed at the light level were verifi ed as possible synaptic connections at the ultrastructural level. Thes e correlated electrophysiological and anatomical studies provide the f irst evidence for connections from pyramid to burst firing interneuron s in the neocortex and indicate that these connections can be mediated by multiple synaptic contacts. The accompanying paper describes the f unctional properties of these connections.