Functional neuromodulation of chemosensation in vertebrates

Abstract

Neuromodulation can be defined as a biophysical process that serves to modify-or modulate-the computation performed by a neuron or network as a function of task demands and behavioral state of the animal. These modulatory effects often involve substances extrinsic to the network under observation, such as acetylcholine (ACh), norepinephrine (NE), histamine, serotonin (5-HT), dopamine (DA), and a variety of neuropeptides. Olfactory and gustatory processes especially need to be adaptive and respond flexibly to changing environments, availability of resources and physiological needs. It is therefore crucial to understand the neuromodulatory processes that regulate the function of these systems.

Figure 1

Schematic depiction of major olfactory and gustatory pathways and their modulatory inputs. Neuromodulatory inputs to structures specifically associated with olfaction or gestation and discussed in this review are depicted. See main text for a describtion of computations in these pathways. The list of structures is not exhaustive and is meant to show the route that information takes before it reaches the primary sensory cortex of each modality.

Figure 2

Illustration of laminar distribution of receptors in the olfactory bulb and cortex with respect to computational functions in these networks. A. Olfactory bulb. Sensory information, transduced by olfactory sensory neurons in the olfactory epithelium (OE) is projected to target neurons in the glomerular layer (GL) of the OB. Local microcircuits, comprised of periglomerular (PG), external tufted (ET) and short axon (SA) cells process the incoming information. This layer of bulbar processing is thought to be involved in contrast and normalization processes. The resulting activity of mitral cells (Mi) is then further processed in the external plexiform layer (EPL), where Mi cells interact with granule cells (Gr). The mutual interactions between these groups of cells and additional interneurons not depicted here are thought to create oscillatory dynamics that serve to synchronize Mi cell outputs towards olfactory secondary cortices. Receptors for ACh, NE and 5HT are numerous and organized in a laminar fashion through out the bulbar layers including GL, EPL, internal plexiform layer (IPL) and granule cell layer (GCL) (nACh: nicotinic, mACh: muscarinic). Bulbar outputs project, among several other structures, to the piriform cortex (PC), where they connect with pyramidal cells (Pyr) and local interneurons (fF) in a widely distributed and non-topographical fashion. A second major class of inhibitory interneurons (Fb) provides additional computational power to this structure. Presynaptic inhibition by metabotropic glutamate receptors in layer Ia mediates a form of short term memory, rapid habituation, whose specificity is dependent on mACh receptors in layers Ia and II. The dense network of association fibers between cortical pyramidal cells has been suggested to form an auto-associative memory capable of storing olfactory information. The modulation of synaptic transmission in this layer by NE and ACh has been shown to be a crucial component of this associative memory function.