Complementary Sensory and Associative Microcircuitry in Primary Olfactory Cortex

Abstract

The three-layered primary olfactory (piriform) cortex is the largest component of the olfactory cortex. Sensory and intracortical inputs converge on principal cells in the anterior piriform cortex (aPC). We characterize organization principles of the sensory and intracortical microcircuitry of layer II and III principal cells in acute slices of rat aPC using laser-scanning photostimulation and fast two-photon population Ca 2ϩ imaging. Layer II and III principal cells are set up on a superficial-to-deep vertical axis. We found that the position on this axis correlates with input resistance and bursting behavior. These parameters scale with distinct patterns of incorporation into sensory and associative microcircuits, resulting in a converse gradient of sensory and intracortical inputs. In layer II, sensory circuits dominate superficial cells, whereas incorporation in intracortical circuits increases with depth. Layer III pyramidal cells receive more intracortical inputs than layer II pyramidal cells, but with an asymmetric dorsal offset. This microcircuit organization results in a diverse hybrid feedforward/recurrent network of neurons integrating varying ratios of intracortical and sensory input depending on a cell's position on the superficial-to-deep vertical axis. Since burstiness of spiking correlates with both the cell's location on this axis and its incorporation in intracortical microcircuitry, the neuronal output mode may encode a given cell's involvement in sensory versus associative processing.

Micro-, Meso- and Macro-Dynamics of the Brain

“…Excitatory neurons in layer 2 can be subdivided in semilunar (upper layer 2) and superficial pyramidal neurons (lower layer 2), whereas those in layer 3 comprise a few deep pyramidal cells and scattered multipolar spiny glutamatergic neurons (Haberly 1983;Suzuki and Bekkers 2006;Bekkers and Suzuki 2013). Although they are embedded in the same basic connectivity scheme, semilunar and superficial pyramidal cells receive different ratios of afferent to associational inputs and may therefore belong to distinct functional sub-circuits (Suzuki and Bekkers 2011; but see Poo and Isaacson 2011), consistent with morphological differences between their dendritic trees and their laminar position (Wiegand et al 2011). Although data on subpopulations of principal cells in DCx are few, analysis of Golgi-stained material also revealed different morphological classes of spiny neurons at different laminar and sublaminar positions in reptilian cortex (Ulinski 1977;Desan 1984) PCx and DCx pyramidal neurons are also similar with respect to their dendritic electrophysiological properties, suggesting comparable integrative properties at the subcellular level (Larkum et al 2008;Bathellier et al 2009).…”

Microcircuits Mediating Feedforward and Feedback Synaptic Inhibition in the Piriform Cortex

“…As noted earlier, SL cells are most likely the first neurons in the feedback inhibitory circuit because they receive the strongest LOT input (Suzuki and Bekkers, 2011;Wiegand et al, 2011). Additional evidence comes from measurements of firing latency.…”

“…We have recently shown that SL cells receive the strongest aff input from the LOT (Suzuki and Bekkers, 2011; see also Wiegand et al, 2011); hence, it is likely that SL cells drive IN2 to generate feedback inhibition (Fig. 1 A).…”

“…The PC is thought to perform a high-level synthetic role by recognizing and remembering odors (Wilson and Stevenson, 2006). Because of its comparatively simple anatomy, together with the fact that its afferent inputs (i.e., the outputs of the bulb) are increasingly well understood, the PC has attracted attention as a model system for the study of cortical sensory processing (Neville and Haberly, 2004;Isaacson, 2005, 2006;Bekkers, 2006, 2011;Barnes et al, 2008;Luna and Schoppa, 2008;Bathellier et al, 2009;Johenning et al, 2009;Poo and Isaacson, 2009;Stettler and Axel, 2009;Stokes and Isaacson, 2010;Wilson, 2010;Davison and Ehlers, 2011;Franks et al, 2011;Poo and Isaacson, 2011;Wiegand et al, 2011). In particular, synaptic inhibition in the PC is of interest because of its likely relevance to olfactory coding and oscillations (Wilson and Bower, 1992;Kay et al, 2009;Isaacson, 2009, 2011;Kay and Beshel, 2010;Zhan and Luo, 2010;Manabe et al, 2011;Zelano et al, 2011).…”

Balanced feedforward inhibition and dominant recurrent inhibition in olfactory cortex

“…In the APC, principal excitatory neuron classes differ in laminar location and in the proportion of afferent vs. intracortical excitatory input received (34)(35)(36)(37). Within L2, semilunar cells (SLCs) receive predominantly afferent excitation, whereas superficial pyramidal cells (sPCs) receive weaker afferent and stronger intracortical excitatory drive.…”