Odour Processing By Principal Neurons of the Piriform Cortex In Vivo

Abstract

The piriform cortex (PC) is important for the cortical processing of olfactory information. The PC is widely viewed as a pattern recognition device whose primary function is the formation of ‘odour objects’, that is, the perception of complex odours comprising many chemical components as single olfactory percepts (e.g. the scent of a rose), a task that is heavily dependent on the intracortical associational network. Two types of glutamatergic principal neurons are present in approximately equal numbers in layer 2 of the PC: semilunar (SL) and superficial pyramidal (SP) cells. Despite a long-standing misconception that the principal neurons of the PC are a functionally homogenous population, recent work has shown that SL and SP cells differ significantly in their connectivity and in vitro electrophysiology. Specifically, emerging data has indicated that intracortical connectivity increases with increasingly deep somatic locations, suggesting that, in response to olfactory stimulation, cortical computations shift from afferent (sensory) processing to associative processing down the PC superficial-to-deep axis. In light of the important differences between the two main classes of principal neurons, we hypothesised that SL and SP cells contribute differentially to the cortical processing of olfactory sensory information.

In this thesis, we examined the odour responses of layer 2 principal neurons in the anterior PC using whole-cell patch clamp electrophysiology. We show that odour responses are highly variable and richly nuanced in vivo; however, they can be broadly separated into three basic categories: excitation, inhibition and unresponsiveness. Our current clamp data revealed that an intrinsic property, the spike after-hyperpolarisation (AHP), correlates strongly with the somatic laminar depth, suggesting that the AHP could be used to identify neurons (SL or SP cells) recorded in vivo. Importantly, current clamp data indicate that olfactory excitatory tuning correlates strongly with the AHP in vivo, such that putative SP cells (characterised by a small AHP) are more broadly excited by odours than putative SL cells (characterised by a large AHP), presumably due to a difference in intracortical connectivity. These results further suggest that, rather than assuming a sharp dichotomy of neuronal phenotypes, SL-like cells gradually transition into SP-like cells along the cortical superficial-to-deep axis.

Voltage clamp data indicate that principal neurons are under a substantial level of tonic inhibition in the absence of odour. We show that spontaneous and odour-evoked inhibition dominates and scales with excitation under physiological conditions. These results suggest that local inhibition contributes to the reported sparse odour coding in the cortex.

Overall, these data are consistent with our proposed model of the anterior PC excitatory network, which posits that 1) principal neuron phenotype transitions smoothly across the cortical superficial-to-deep axis and 2) principal neurons become increasingly incorporated into the local intracortical microcircuits with increasingly deep somatic location, as a result, 3) neuronal excitatory tuning becomes progressively broader with increasing somatic depth. These results suggest that SL cells may be important for decorrelating overlapping input patterns and hence preserving the salient olfactory attributes of an odour, whereas SP cells are more heavily implicated in the associative aspect of olfactory processing.