All in a Sniff: Olfaction as a Model for Active Sensing

Department of Physiology and Brain Institute, University of Utah, Salt Lake City, UT 84103, USA.
Neuron (Impact Factor: 15.05). 09/2011; 71(6):962-73. DOI: 10.1016/j.neuron.2011.08.030
Source: PubMed

ABSTRACT Sensation is an active process involving the sampling and central processing of external stimuli selectively in space and time. Olfaction in particular depends strongly on active sensing due to the fact that-at least in mammals-inhalation of air into the nasal cavity is required for odor detection. This seemingly simple first step in odor sensation profoundly shapes nearly all aspects of olfactory system function, from the distribution of odorant receptors to the functional organization of central processing to the perception of odors. The dependence of olfaction on inhalation also allows for profound modulation of olfactory processing by changes in odor sampling strategies in coordination with attentional state and sensory demands. This review discusses the role of active sensing in shaping olfactory system function at multiple levels and draws parallels with other sensory modalities to highlight the importance of an active sensing perspective in understanding how sensory systems work in the behaving animal.

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Available from: Matt Wachowiak, Mar 24, 2014
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    • "We propose that volition may therefore be a primitive capability of vertebrate brains that precedes the advanced cognitive capacities of primates. Animals actively sample their environment using, for example, whisking, sniffing and saccadic eye movements; these active sensing behaviours (Nelson and MacIver, 2006; Kleinfeld et al., 2006; Otero-Millan et al., 2008; Wachowiak, 2011) occur more frequently during periods of active exploration (Poulet and Petersen, 2008; Schroeder et al., 2010). "
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    ABSTRACT: Cortical activity precedes self-initiated movements by several seconds in mammals; this observation has led into inquiries on the nature of volition. Preparatory neural activity is known to be associated with decision making and movement planning. Self-initiated locomotion has been linked to increased active sensory sampling; however, the precise temporal relationship between sensory acquisition and voluntary movement initiation has not been established. Based on long-term monitoring of sensory sampling activity that is readily observable in freely behaving pulse-type electric fish, we show that heightened sensory acquisition precedes spontaneous initiation of swimming. Gymnotus sp. revealed a bimodal distribution of electric organ discharge rate (EODR) demonstrating down- and up-states of sensory sampling and neural activity; movements only occurred during up-states and up-states were initiated before movement onset. EODR during voluntary swimming initiation exhibited greater trial-to-trial variability than the sound-evoked increases in EODR. The sampling variability declined after voluntary movement onset as previously observed for the neural variability associated with decision making in primates. Spontaneous movements occurred randomly without a characteristic timescale, and no significant temporal correlation was found between successive movement intervals. Using statistical analyses of spontaneous exploratory behaviours and associated preparatory sensory sampling increase, we conclude that electric fish exhibit key attributes of volitional movements, and that voluntary behaviours in vertebrates may generally be preceded by increased sensory sampling. Our results suggest that comparative studies of the neural basis of volition may therefore be possible in pulse-type electric fish, given the substantial homologies between the telencephali of teleost fish and mammals.
    Journal of Experimental Biology 10/2014; 217(Pt 20):3615-28. DOI:10.1242/jeb.105502 · 2.90 Impact Factor
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    • "However , recent studies have shown a much more complex scenario in awake animals, requiring re-evaluation of our notions of olfactory processing (Kato et al., 2012; Wachowiak et al., 2013). MCs in awake, behaving animals are spontaneously active (Rinberg and Gelperin, 2006; Rinberg et al., 2006; Davison and Katz, 2007) with firing that is often locked to the respiration cycle (Cury and Uchida, 2010; Wachowiak, 2011). Odor-evoked responses are not encoded in simple changes in firing frequencies; instead, the OB adopts various sophisticated mechanisms, involving the activity of MCs, to detect and encode odors. "
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    ABSTRACT: The tractable, layered architecture of the olfactory bulb (OB), and its function as a relay between odor input and higher cortical processing, makes it an attractive model to study how sensory information is processed at a synaptic and circuit level. The OB is also the recipient of strong neuromodulatory inputs, chief among them being the central cholinergic system. Cholinergic axons from the basal forebrain modulate the activity of various cells and synapses within the OB, particularly the numerous dendrodendritic synapses, resulting in highly variable responses of OB neurons to odor input that is dependent upon the behavioral state of the animal. Behavioral, electrophysiological, anatomical, and computational studies examining the function of muscarinic and nicotinic cholinergic receptors expressed in the OB have provided valuable insights into the role of acetylcholine (ACh) in regulating its function. We here review various studies examining the modulation of OB function by cholinergic fibers and their target receptors, and provide putative models describing the role that cholinergic receptor activation might play in the encoding of odor information.
    Frontiers in Synaptic Neuroscience 09/2014; 6:21. DOI:10.3389/fnsyn.2014.00021
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    • "To increase their survival strategies and fitness, adaptation of the air-breathing pathway in nasal cavities as well as the general nose morphology itself have facilitated this specific olfactory detection (Negus, 1954; Harkema, 1991; Harkema et al., 2006; Rae et al., 2006). This environmental adaptation is especially significant for the most rostral part of the rodent wet-snout, the so-called rhinarium (Hill, 1948; Ade, 1999), which is implicated both in tactile and active olfactory sensing (sniffing behavior) (Wachowiak, 2011; Haidarliu et al., 2012, 2013) and is directly dependent of the environmental context such as temperature variations (Ade, 1999; Ince et al., 2012; Brechbühl et al., 2013a; Cilulko et al., 2013). "
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    ABSTRACT: In the mouse, the Grueneberg ganglion (GG) is an olfactory subsystem implicated both in chemo- and thermo-sensing. It is specifically involved in the recognition of volatile danger cues such as alarm pheromones and structurally-related predator scents. No evidence for these GG sensory functions has been reported yet in other rodent species. In this study, we used a combination of histological and physiological techniques to verify the presence of a GG and investigate its function in the rat, hamster and gerbil comparing with the mouse. By scanning and transmitted electron microscopy, we found isolated or groups of large GG cells of different shapes that in spite of their gross anatomical similarities, display important structural differences between species. We performed a comparative and morphological study focusing on the conserved olfactory features of these cells. We found fine ciliary processes, mostly wrapped in ensheating glial cells, in variable number of clusters deeply invaginated in the neuronal soma. Interestingly, the glial wrapping, the amount of microtubules and their distribution in the ciliary processes were different between rodents. Using immunohistochemistry, we were able to detect the expression of known GG proteins, such as the membrane guanylyl cyclase G and the cyclic nucleotide-gated channel A3. Both the expression and the subcellular localization of these signaling proteins were found to be species-dependent. Calcium imaging experiments on acute tissue slice preparations from rodent GG demonstrated that the chemo- and thermo-evoked neuronal responses were different between species. Thus GG neurons from mice and rats displayed both chemo- and thermo-sensing, while hamsters and gerbils showed profound differences in their sensitivities. We suggest that the integrative comparison between the structural morphologies, the sensory properties and the ethological contexts supports species-dependent GG features prompted by the environmental pressure
    Frontiers in Neuroanatomy 08/2014; 8. DOI:10.3389/fnana.2014.00087 · 3.54 Impact Factor
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