MEMBRANE CURRENTS EVOKED BY AFFERENT FIBER STIMULATION IN RAT PIRIFORM CORTEX .1. CURRENT SOURCE-DENSITY ANALYSIS

1. The membrane currents evoked by afferent fiber stimulation in the piriform cortex were derived by the use of current source-density (CSD) analysis in the rat under urethan anesthesia. The primary goals were to test hypotheses concerning the sequence of synaptic events evoked by afferent fiber stimulation and to derive data required for development and testing of the model presented in the companion paper. 2. In confirmation of previous studies, it was found that afferent fiber stimulation evokes a monosynaptic excitatory postsynaptic current (EPSC) in distal segments of pyramidal cell apical dendrites (layer Ia) followed by a strong disynaptic EPSC in adjacent middle segments (superficial layer Ib). 3. Given the central importance of the strong disynaptic EPSC in models for operation of the piriform cortex, the hypothesis that it is mediated by long association fibers from the anterior piriform cortex was tested by comparing its latency in response to stimulation at anterior and posterior locations. The results confirmed the hypothesis and ruled out a significant contribution from local connections in the posterior piriform cortex. 4. Intensification of pyramidal cell activity by spatially restricted disinhibition with picrotoxin confirmed the hypothesis that associational projections from the posterior piriform cortex can mediate a long-latency disynaptic EPSC in proximal dendritic segments (mid to deep layer Ib) in the anterior piriform cortex. 5. Analysis of the time course of the monosynaptic EPSC in different areas revealed that activation of the anterior piriform cortex from afferent fiber stimulation is fast and nearly synchronous throughout its extent as a result of the relatively high conduction velocities of afferent fibers in the lateral olfactory tract (LOT). By contrast, the posterior piriform cortex is sequentially activated by this EPSC as a consequence of the slow propagation velocity of afferent fiber collaterals that course across its surface. This activation is sufficiently slow that a large phase lag is present between rostral and caudal regions. 6. The time courses of the monosynaptic and principal disynaptic EPSCs changed in characteristically different ways with increasing distance from the LOT within the posterior piriform cortex. Simulations in the companion paper indicate that initiation and propagation patterns for activity in fiber systems rather than differences in synaptic conductance waveforms are responsible for these differences. 7. Although the laminar distribution of the active inward current component of the monosynaptic EPSC remained constant over time, the peak outward current associated with this EPSC shifted from the depth of proximal apical dendrites (layer Ib) to the depth of superficial pyramidal cell somata (layer II). The previous hypothesis that the onset of the disynaptic Cl--mediated inhibitory postsynaptic current in pyramidal cell somata contributes to this shift was not confirmed. Evidence included the demonstration of an identical shift in the response to the second of a pair of shocks when disynaptic events were blocked. Simulations in the companion paper suggest that passive properties of pyramidal cells alone account for this shift. 8. Two observations have implications for the interpretation of field potentials: as a result of the shift in depth of outward current, the amplitude of the evoked potential associated with the mono-synaptic EPSC was approximately twofold greater during the falling phase than during the rising phase at times when membrane currents were equal. This result indicates that there can be a substantial difference between the time course of field potentials and the underlying membrane currents. A second consequence of the shift in location of return current was that the evoked potential associated with the isolated monosynaptic EPSC was biphasic at intermediate depths in the cortex. Such biphasic potentials have been assumed to reflect the presence of more than one active process. 9. High resolution CSD analysis of period 3 revealed an inward current at the depth of distal apical dendrites (layer Ia) and out-ward currents at the depth of mid to proximal apical dendrites (layer Ib) and basal dendrites (layer III). No direct evidence was obtained concerning the identity of these currents, although correlational arguments suggest contributions from reactivation of afferent fibers after the cessation of inhibition and from the K+-mediated inhibitory postsynaptic potential in pyramidal cell dendrites.