Elsevier

Current Opinion in Neurobiology

Volume 40, October 2016, Pages 170-177
Current Opinion in Neurobiology

Neuromodulation of olfactory transformations

https://doi.org/10.1016/j.conb.2016.07.006Get rights and content

Highlights

  • Neuromodulators are widely represented throughout olfactory networks.

  • Neuromodulators have diverse actions on cortical circuits.

  • Olfactory computations are overlapping and interact with each other.

  • Functional effects of neuromodulators cannot be simple assigned a function.

  • Cellular effects of diverse neuromodulators overlap in olfactory networks.

The olfactory bulb and piriform cortex are the best studied structures of the mammalian olfactory system and are heavily innervated by extrinsic neuromodulatory inputs. The state-dependent release of acetylcholine, norepinephrine, serotonin, and other neuromodulators into these olfactory structures alters a constellation of physiological parameters in neurons and synapses that together modify the computations performed on sensory signals. These modifications affect the specificity, detectability, discriminability, and other properties of odor representations and thereby govern perceptual performance. Whereas different neuromodulators have distinct cellular effects, and tend to be associated with nominally different functions, it also is clear that these purported functions overlap substantially, and that ad hoc hypotheses regarding the roles of particular neuromodulators may have reached the limits of their usefulness.

Introduction

Neuromodulation can be defined as a neurochemical process that serves to modify (modulate) the computations performed by a neuron or network as a function of task demands or behavioral state. This modulation can be mediated by neurochemicals arising from extrinsic sources (including acetylcholine from basal forebrain nuclei, norepinephrine from the locus coeruleus, and other amines and peptides), as well as those released from neurons intrinsic to a local network (including ancillary effects of classical neurotransmitters mediated by metabotropic receptors as well as the release or co-release of aminergic or peptide neuromodulators). While the functional distinction between neurotransmitters and neuromodulators is imperfect, the latter are characterized by effects that are best understood as changes in neuronal or network state that alter responsivity to synaptic inputs.

Olfactory networks (Figure 1) are constructed to extract and recognize pertinent signals from unpredictable, chemically noisy environments, and must be able to adapt flexibly to changes in the sensory environment as well as to internal state variables such as hunger or alarm. These adaptive transformations are often regulated by neuromodulatory inputs, a wide variety of which innervate the olfactory system. Consequently, the olfactory system has served as an important model system for understanding the functional roles and computational mechanisms of neuromodulation, particularly in mammals. One of its advantages in this role is that there has been somewhat less of a tendency to associate individual neuromodulators with broad behavioral states such as attention or arousal. While these relationships may have merit, their presumption also can introduce bias into experimental design and interpretation. In contrast, the construction of multiscale models of neuromodulation can elucidate the relationships between cellular and synaptic effects and the resulting systems-level transformations of (sensory) input, providing rich insights into the complexity and contingencies of neural circuit function. We here review some examples of the neuromodulatory regulation of specific functional computations hypothesized for olfactory circuitry in adult rodents.

Section snippets

Olfactory processing and neuromodulation

Chemical signals are transduced by primary olfactory sensory neurons (OSNs) in the nasal cavities, which project directly to the central nervous system to form discrete neuropilar glomeruli within the olfactory bulb (OB). Within these glomeruli, OSN axonal arbors interact with mitral and tufted cells (principal neurons) along with several local interneuron species that together form glomerular microcircuits (reviewed in [1, 2]). Computational studies of experimental data have shown that these

Synthesis

Neuromodulators regulate olfactory networks and modify their computational transformations at multiple processing stages. Whereas the individual cellular effects of different neuromodulators clearly differ, some of their observed functional effects on network processing appear similar or closely integrated. Nevertheless, the functional effects of different modulators tend to be labeled differently, partially for historical reasons, even when their concrete effects are difficult to distinguish.

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

References (46)

  • L.B. Haberly et al.

    Olfactory cortex: model circuit for study of associative memory?

    Trends Neurosci

    (1989)
  • R.J. Stevenson et al.

    Odour perception: an object-recognition approach

    Perception

    (2007)
  • D.A. Wilson et al.

    Neurobiology of a simple memory

    J Neurophysiol

    (2008)
  • M.L. Fletcher et al.

    Neural correlates of olfactory learning: critical role of centrifugal neuromodulation

    Learn Memory

    (2010)
  • R.D. D'Souza et al.

    Paying attention to smell: cholinergic signaling in the olfactory bulb

    Front Synap Neurosci

    (2014)
  • L. de Almeida

    Computational modeling suggests distinct, location-specific function of norepinephrine in olfactory bulb and piriform cortex

    Front Comput Neurosci

    (2015)
  • G. Li et al.

    A two-layer biophysical model of cholinergic neuromodulation in olfactory bulb

    J Neurosci

    (2013)
  • T.A. Cleland et al.

    Non-topographical contrast enhancement in the olfactory bulb

    BMC Neurosci

    (2006)
  • D. Chaudhury et al.

    Bulbar acetylcholine enhances neural and perceptual odor discrimination

    J Neurosci

    (2009)
  • N. Mandairon

    Cholinergic modulation in the olfactory bulb influences spontaneous olfactory discrimination in adult rats

    Eur J Neurosci

    (2006)
  • R.T. Pressler et al.

    Muscarinic receptor activation modulates granule cell excitability and potentiates inhibition onto mitral cells in the rat olfactory bulb

    J Neurosci

    (2007)
  • G. Li et al.

    Functional differentiation of cholinergic and noradrenergic modulation in a biophysical model of olfactory bulb granule cells

    J Neurophysiol

    (2015)
  • S. Devore et al.

    Noradrenergic and cholinergic modulation of olfactory bulb sensory processing

    Front Behav Neurosci

    (2012)
  • Cited by (0)

    View full text