Olfactory maps, circuits and computations

Abstract

Sensory information in the visual, auditory and somatosensory systems is organized topographically, with key sensory features ordered in space across neural sheets. Despite the existence of a spatially stereotyped map of odor identity within the olfactory bulb, it is unclear whether the higher olfactory cortex uses topography to organize information about smells. Here, we review recent work on the anatomy, microcircuitry and neuromodulation of two higher-order olfactory areas: the piriform cortex and the olfactory tubercle. The piriform is an archicortical region with an extensive local associational network that constructs representations of odor identity. The olfactory tubercle is an extension of the ventral striatum that may use reward-based learning rules to encode odor valence. We argue that in contrast to brain circuits for other sensory modalities, both the piriform and the olfactory tubercle largely discard any topography present in the bulb and instead use distributive afferent connectivity, local learning rules and input from neuromodulatory centers to build behaviorally relevant representations of olfactory stimuli.

Figure 1. General Anatomy of the Mammalian Olfactory System

A) Anatomy of the peripheral olfactory system. Odorant sensory neurons (OSNs) distributed across the nasal epithelium express a single odorant receptor (OR). Every OSN expressing a particular OR sends its axons to a genetically stereotyped location on the surface of the olfactory bulb, termed a glomerulus (dashed circles). The bulb contains a number of interneuron types (yellow) including periglomerular and granule cells. Mitral and the more superficial tufted cells (M/T) send their dendrites into a single glomerulus and their axons fasciculate to form the lateral olfactory tract (LOT), which projects to olfactory cortex. As noted in the text this review focuses on feedforward afferents to the olfactory cortex; for simplicity this diagram therefore excludes the many cell types and wiring relevant to intrabulbar processing of olfactory information. B) Axonal projection patterns in olfactory cortex from a single glomerulus. Top, flattened preparation of olfactory cortex with nuclei stained in blue. Major sub-regions of the olfactory cortex are outlined and labeled: piriform cortex (PIR), olfactory tubercle (OT), anterior olfactory nucleas (AON), cortical amygdala (AMG), lateral entorhineal cortex (ENT). Bottom, same preparation where a single glomerulus has been electroporated with TMR-dextran (pink). Each sub-region of the olfactory cortex is innervated, but projection patterns vary extensively from region to region. Scale bar 700 um; A, anterior; P, posterior; D, dorsal; V, ventral. Figure from [39].

Figure 2. Microcircuits of the Piriform Cortex and Olfactory Tubercle

A) Major cell types and anatomy of the Piriform Cortex. Excitatory neurons are colored in blue, inhibitory neurons in red. Axons from the LOT are restricted to layer 1a, where they synapse onto spiny pyramidal cells (SP), semilunar cells (SL) and interneurons such as horizontal cells (HZ). Interneurons present in layer 1a provide feedforward inhibition to SL/SP cells. Collaterals of SP and SL axons ramify extensively across layers 1b through 3. These collaterals excite other SP cells as well as small and large multipolar neurons (MP_S, MP_L). Multiform neurons provide strong feedback inhibition that balances excitation and keeps odor representations sparse. Dendrites are represented by thick lines, axons as thin lines. B) Major cell types and anatomy of the Olfactory Tubercle. Axons from the LOT are restricted primarily to the superficial molecular layer of the OT. There, they synapse onto the dendrites of D1R- and D2R-type medium spiny neurons (MSNs, D1 colored in light red, D2 in dark red). The somata of these cells are located in the dense cell layer (DCL), which undulates across the extent of the OT. Also present are various interneuron types, such as crescent cells (CC, green). Below the DCL in the multiform layer are tight clusters of granule cells, the Islands Of Cajella (IC). The ICs displace the DCL to form crests that approach the pial surface containing dwarf cells (DC). Intermingled within the multiform layer are other MSNs and regions of ventral pallidum and displaced pallidal cells (PD, orange).

Figure 3. Odor Representations and Learning in the Piriform Cortex

A) Odor representations in the Piriform Cortex. Distributed input from the olfactory bulb activates unique, overlapping and sparse patterns of neuronal activation across the extent of the piriform cortex, ideal for encoding odor identity. Semilunar cells are especially strongly activated by afferent input from the bulb (circles), while spiny pyramidal cells (triangles) are excited primarily by local network activity. Ensembles for two distinct odors (A and B) are shown, active cells are colored. B) Odor mixtures are dynamically learned and stabilized by Acetylcholine. When presented with a mixture of odors (A + B), activity at new excitatory and inhibitory synapses drive some previously silent neurons to fire (double triangles) and some previously excited cells to fall silent (grey centers). The presence of acetylcholine in the piriform allows for rapid synaptic plasticity, which stabilizes the representation of A+B as a unique odor object. Note that the semilunar cells remain activated, while spiny pyramidal cells are added and lost in the new representation.