Membrane currents evoked by afferent fiber stimulation in rat piriform cortex. I. Current source-density analysis

Abstract

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).(ABSTRACT TRUNCATED AT 400 WORDS)

Odor-Driven Activity in the Olfactory Cortex of an In Vitro Isolated Guinea Pig Whole Brain With Olfactory Epithelium

“…CSD analysis demonstrated that the onset of the odorinduced Ib sink (period 1) was followed by a small sink in layer II-III coupled to a reinforcement of the Ib sink. In line with the previous studies by the Haberly group, the layer II-III sink could be attributed to an inhibitory, possibly feedback, potential (Ketchum and Haberly 1993b;Neville and Haberly 2004). Even though the definitive confirmation of the existence of an inhibitory component in the response could be attained by intracellular recordings, extracellular unit recordings performed in our study strongly support this conclusion.…”

“…The laminar profile of LFPs obtained by LOT stimulation in this preparation (Fig. 3A) was very similar to those described in the previous studies (Biella et al 1996a,b;Ketchum and Haberly 1993b). Then, we compared the initial component of the odor-induced response with LOT-evoked response sequentially recorded at identical cortical depths.…”

“…Twelve-channel electrodes (homemade) were also utilized to record LFPs simultaneously at the depth of 0 -1,100 m in 100-m intervals. To perform the CSD analysis, second derivative was calculated at each recording depth (Ketchum and Haberly 1993b). For cortical micro-stimulation to the rostral part of APC (APCvr) and the anterior olfactory cortex (AOC), bipolar tungsten electrodes were positioned at cell body layer of those cortices.…”

“…In layer II, inhibitory interneurons receive excitatory input and form synapses with cell bodies of pyramidal cells (feedback inhibition) (Biedenbach and Stevens 1969;Haberly 1973;Satou et al 1983). This highly ordered neuronal system allows the visualization of spatial and temporal sequences of extracellular current sinks and sources associated with membrane currents in dendrites by current source-density (CSD) analysis of laminar field potential profiles (Ketchum and Haberly 1993b;Mitzdorf 1985).…”

Complementary Sensory and Associative Microcircuitry in Primary Olfactory Cortex

“…More recently, these concepts have been merged into the proposition of the anterior piriform cortex (aPC) as a "hybrid recurrent/feedforward pattern correlation network" (Haberly, 2001). In vivo current source density analysis in the aPC revealed the sequential activation of sensory and intracortical synapses on aPC principal cells (Ketchum and Haberly, 1993).…”