Intrinsic and Extrinsic Neuromodulation of Olfactory Processing

Abstract

Neuromodulation is a ubiquitous feature of neural systems, allowing flexible, context specific control over network dynamics. Neuromodulation was first described in invertebrate motor systems and early work established a basic dichotomy for neuromodulation as having either an intrinsic origin (i.e., neurons that participate in network coding) or an extrinsic origin (i.e., neurons from independent networks). In this conceptual dichotomy, intrinsic sources of neuromodulation provide a “memory” by adjusting network dynamics based upon previous and ongoing activation of the network itself, while extrinsic neuromodulators provide the context of ongoing activity of other neural networks. Although this dichotomy has been thoroughly considered in motor systems, it has received far less attention in sensory systems. In this review, we discuss intrinsic and extrinsic modulation in the context of olfactory processing in invertebrate and vertebrate model systems. We begin by discussing presynaptic modulation of olfactory sensory neurons by local interneurons (LNs) as a mechanism for gain control based on ongoing network activation. We then discuss the cell-class specific effects of serotonergic centrifugal neurons on olfactory processing. Finally, we briefly discuss the integration of intrinsic and extrinsic neuromodulation (metamodulation) as an effective mechanism for exerting global control over olfactory network dynamics. The heterogeneous nature of neuromodulation is a recurring theme throughout this review as the effects of both intrinsic and extrinsic modulation are generally non-uniform.

Elevated CO2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon (Oncorhynchus kisutch)

“…Inhibitory GABAergic neurons in the olfactory bulb play a critical role in synchronization and regulation of neuronal signals required for appropriate odor discrimination (Lizbinski & Dacks, ; Tabor, Yaksi, & Friedrich, ). The lack of observed effects of CO 2 in the olfactory epithelium and some discrete regions of the olfactory bulb may be due to differential spatial distribution of GABAergic neurons and GABA receptors within these tissues and the role of GABAergic neurons in regulating signaling of specific odorants and mixtures (Cocco et al, ; Lizbinski & Dacks, ; McGann, ; Tabor et al, ). For example, while G protein‐coupled GABA B receptors are present in the axonal presynaptic region of the olfactory sensory neurons within the olfactory bulbs, GABA A receptors are broadly present on mitral/tufted cell secondary neurons within the olfactory bulb (McGann, ; Tan, Savigner, Ma, & Luo, ).…”

“…Our EEG recordings support this hypothesis, as elevated CO 2 exposures increased the amplitude, and tended to increase the dura- It has been hypothesized that the main mechanism of behavioral disruption by elevated CO 2 exposure is via alteration of GABA signaling in the central nervous system, driven by a reversal of the Cl − / HCO 3 + membrane gradient and a linked disruption of the normal inhibitory action of the GABA A receptor (Nilsson et al, 2012). The and regulation of neuronal signals required for appropriate odor discrimination (Lizbinski & Dacks, 2017;Tabor, Yaksi, & Friedrich, 2008). The lack of observed effects of CO 2 in the olfactory epithelium and some discrete regions of the olfactory bulb may be due to differential spatial distribution of GABAergic neurons and GABA receptors within these tissues and the role of GABAergic neurons in regulating signaling of specific odorants and mixtures (Cocco et al, 2017;Lizbinski & Dacks, 2017;McGann, 2013;Tabor et al, 2008).…”

“…The and regulation of neuronal signals required for appropriate odor discrimination (Lizbinski & Dacks, 2017;Tabor, Yaksi, & Friedrich, 2008). The lack of observed effects of CO 2 in the olfactory epithelium and some discrete regions of the olfactory bulb may be due to differential spatial distribution of GABAergic neurons and GABA receptors within these tissues and the role of GABAergic neurons in regulating signaling of specific odorants and mixtures (Cocco et al, 2017;Lizbinski & Dacks, 2017;McGann, 2013;Tabor et al, 2008).…”

Neuromodulation and Differential Learning Across Mosquito Species

“…Dopaminergic modulation in olfactory learning has primarily been studied in the mushroom bodies [22][23][24] , which receive afferents from the ALs and integrate signals from different senses as well as reward and punishment. However, neuromodulation at the level of the AL can induce neuroplasticity, mediate gain control of olfactory signals, and change the strength of output to higherorder centers like the mushroom bodies 25 . In Ae.…”

Regulation of modulatory cell activity across olfactory structures in Drosophila melanogaster

“…Virtually all neuronal circuits are subject to neuromodulation from both neurons intrinsic to a network and extrinsic centrifugal sources (1,2). In vertebrates, extrinsic modulation is often supplied by nuclei located deep within the brainstem that release a variety of transmitters such as norepinephrine (NE) (3), serotonin (5-HT) (4,5), dopamine (DA) (6,7), or acetylcholine (Ach) (8).…”