New Features of Connectivity in Piriform Cortex Visualized by Intracellular Injection of Pyramidal Cells Suggest that “Primary” Olfactory Cortex Functions Like “Association” Cortex in Other Sensory Systems

Abstract

Associational connections of pyramidal cells in rat posterior piriform cortex were studied by direct visualization of axons stained by intracellular injection in vivo. The results revealed that individual cells have widespread axonal arbors that extend over nearly the full length of the cerebral hemisphere. Within piriform cortex these arbors are highly distributed with no regularly arranged patchy concentrations like those associated with the columnar organization in other primary sensory areas (i.e., where periodically arranged sets of cells have common response properties, inputs, and outputs). A lack of columnar organization was also indicated by a marked disparity in the intrinsic projection patterns of neighboring injected cells. Analysis of axonal branching patterns, bouton distributions, and dendritic arbors suggested that each pyramidal cell makes a small number of synaptic contacts on a large number (Ͼ1000) of other cells in piriform cortex at disparate locations. Axons from individual pyramidal cells also arborize extensively within many neighboring cortical areas, most of which send strong projections back to piriform cortex. These include areas involved in high-order functions in prefrontal, amygdaloid, entorhinal, and perirhinal cortex, to which there are few projections from other primary sensory areas. Our results suggest that piriform cortex performs correlative functions analogous to those in association areas of neocortex rather than those typical of primary sensory areas with which it has been traditionally classed. Findings from other studies suggest that the olfactory bulb subserves functions performed by primary areas in other sensory systems. Key words: piriform cortex; olfactory cortex; cortico-cortical; olfaction; association cortex; neural networksPiriform cortex has long been considered as "primary" olfactory cortex because it is the largest area that receives direct input from the olfactory bulb (OB), the structure that monosynaptically relays input from olfactory receptor neurons. However, physiological and anatomical studies suggest that this cortical area is organized in a fundamentally different way than the primary cortical areas for nonchemical senses (Haberly, 1998). Physiological studies have shown that neurons in piriform cortex typically respond in varying degree to odorant molecules with a broad range of structure (Tanabe et al., 1975;Schoenbaum and Eichenbaum, 1995), in contrast to the exquisite selectivity exhibited by cells in primary sensory areas in neocortex. Studies with extracellularly injected axon tracers have shown that associational (cortico-cortical) projections from restricted regions of piriform cortex are highly distributed spatially, both within piriform cortex and in other olfactory cortical areas (Haberly and Price, 1978;Luskin and Price, 1983). This contrasts with the topographically ordered, columnar architecture of the other primary sensory areas in rat and higher mammals (Chapin et al., 1987;Malach, 1989;Ojima et al., 1991), and is reminiscent of so-...

Synaptic Integration of Olfactory Information in Mouse Anterior Olfactory Nucleus

“…Alternatively, this transform may be mediated by intracortical or corticocortical connections through the well developed association fiber network (Neville and Haberly, 2004). Intracellular staining of single olfactory cortical neurons reveals that their synaptic terminals ramify broadly throughout the entire olfactory cortex (Luskin and Price, 1983a,b;Ojima et al, 1984;Johnson et al, 2000), providing the likely source of the disynaptic EPSPs evoked in olfactory cortical neurons by electrical stimulation of the LOT (Neville and Haberly, 2004). Therefore, abundant synaptic substrates for both direct and indirect convergence exist between the MOB and the AON and could account for the broad patterns of synaptic responsiveness in AON neurons we detected.…”

Beta- and gamma-frequency coupling between olfactory and motor brain regions prior to skilled, olfactory-driven reaching

“…For instance, this task is known to be olfactory-driven (Whishaw and Tomie 1989). We therefore chose to record from the paleocortical pPIR because it is the main output region of the extended olfactory system (Litaudon et al 1997;Haberly 2001) and it monosynaptically projects to the orbitofrontal cortex, entorhinal cortex, basolateral amygdala, and other sites involved in motivationally based decision-making (Johnson et al 2000;Haberly 2001). Also, the pPIR has been strongly implicated in complex odor task learning (Chabaud et al 1999;Haberly 2001;Mouly and Gervais 2002), that in rats is thought to be on a par with the executive-task abilities displayed by primates in the visual and auditory domains (Otto and Eichenbaum 1992;Dusek and Eichenbaum 1997;Dusek and Eichenbaum 1998;Schoenbaum and Setlow 2001).…”

The fundamental role of memory in olfactory perception

“…3). The anatomical basis for such synthesis exists both in the projection of mitral cells conveying receptorspecific input that converges in overlapping terminal patches on the anterior piriform cortex [43] and, perhaps more importantly, through the extensive intracortical association-fiber system [44]. Experience with an odor (or odor mixture) in a variety of conditions allows that odor-specific activity pattern to be synthesized as a unique perceptual whole through cortical synaptic plasticity and, furthermore, allows that pattern to be subsequently recognized against other background patterns of activity or during partial input degradation [39,45].…”