Odor Perception and Olfactory Bulb Plasticity in Adult Mammals

Abstract

Mandairon N, Linster C. Odor perception and olfactory bulb plasticity in adult mammals. J Neurophysiol 101: 2204 -2209, 2009. First published March 4, 2009 doi:10.1152/jn.00076.2009. The adult mammalian olfactory bulb (OB) is unique in that olfactory sensory neurons project directly, without prior thalamic relay, to the OB. This review discusses evidence for the direct involvement of the OB in odor perception and its modulation by olfactory experience. We first discuss recent data showing that the OB exhibits a high level of plasticity in response to olfactory experience including exposure, enrichment, and learning. We next review evidence showing that, in return, experimental manipulation of the OB neural network changes how odorants are processed and perceived. We finally review in more detail a few experiments showing a tight correlation between the modulation of OB neural processing and odor perception. We argue that the OB has evolved to be an adapting network, allowing animals to adjust olfactory computations to changing environments. I N T R O D U C T I O NSensory processing involves a hierarchy of interconnected sensory, cortical, and subcortical areas. When discussing these hierarchies and interactions, olfactory processing is often set apart due to the lack of direct thalamic pathways between sensory and cortical processing areas. Indeed, olfactory signals, after being received and transformed by sensory neurons, are projected directly to an anatomically well studied cortical structure-the olfactory bulb (OB)-with projections to the thalamus established further downstream of the pathway. A recent review has compared the OB to the thalamus in its functional signal processing properties (Kay and Sherman 2007) and discussed how both structures act as early processing stages in which cortical and modulatory feedback can substantially shape sensory representations. Here, we review recent evidence showing that, indeed, the OB is more than a relay station or a feedforward filter but rather actively shapes, and is actively shaped by, olfactory perception-a notion introduced Ͼ20 yr ago by Freeman and Schneider (1982). A crucial component of this function constitutes the central projections to the OB, including cortical, subcortical, and modulatory projections (reviewed in Shipley and Ennis 1996) (Fig. 1). We discuss data showing how olfactory experience changes the OB network and how manipulations of the OB network change odor perception on several timescales. We finally review in more detail a few experiments showing a tight correlation between the modulation of OB neural activity and odor perception. Literature pertaining to neonatal olfactory learning has been intensely and clearly reviewed elsewhere

Extinction reverses olfactory fear-conditioned increases in neuron number and glomerular size

“…Mechanisms related to altered cell turnover of OSNs may play an important role. Previous work has shown that associative olfactory learning modulates the survival of newborn neurons and increases the survival of adultborn neurons in the OB (29)(30)(31)(32). Although these studies investigated the contribution of olfactory neurogenesis to learning at the level of the OB, learning-dependent regulation of epithelial olfactory neurogenesis, in which OSNs are in direct contact with environmental cues, may play a similarly and perhaps even greater role in shaping sensory epithelial responses to learning.…”

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

“…One striking feature of the olfactory system is the large amount of centrifugal influence on odor processing in the early olfactory pathways (Fletcher and Chen 2010;Mandairon and Linster 2009). The mammalian OB receives massive cholinergic inputs from the basal forebrain and dense noradrenergic innervations from the locus coeruleus, both of which have profound effects on odor processing as well as on olfactory learning and memory Linster et al 2011).…”

Nonlinear effects of noradrenergic modulation of olfactory bulb function in adult rodents

“…The olfactory bulb is believed to filter and transform these incoming sensory data, performing normalization, contrast enhancement, signal-to-noise regulations, and other types of operations before conveying the processed olfactory information to several different secondary olfactory structures via mitral/tufted cell axon collaterals (Cleland and Linster 2003). Neuromodulatory inputs such as NE, acetylcholine, and serotonin modulate and change these functions of the olfactory bulb, presumably adapting the performed computations to maximize processing dependent on the specific behavioral demands on the animal (reviewed in Mandairon and Linster 2009). …”

“…Modulatory inputs acting on the excitability and synaptic interactions in these bulbar layers could therefore change these computations and modulate the degree of contrast enhancement performed in a given behavioral situation. Behavioral data in which modulatory functions in the MOB have been disturbed clearly point to contrast enhancement being an important function of the MOB (reviewed in Mandairon and Linster 2009). For example, enhancing cholinergic activity in the MOB increased rats' ability to discriminate between chemically very similar odorants, whereas blockade of cholinergic receptors decreased this discrimination; these results can be predicted by known effects of cholinergic inputs onto glomerular circuits mediating contrast (Chaudhury et al 2009;Linster and Cleland 2002;Mandairon et al 2006a).…”