Chapter 8 - Coding Odor Identity and Odor Value in Awake Rodents
Introduction
One of the most substantial questions remaining in olfactory processing is how changes in neuronal activity encode information on sensory input and gate sensory decision making. With a few interesting exceptions, in the past, the majority of studies involved extracellular signal recording or imaging studies in the olfactory bulb (OB) of anesthetized animals (Pain et al., 2011, Rinberg and Gelperin, 2006). However, in recent years, evidence has suggested that in awake animals odor coding is dramatically different depending on behavioral status. Indeed, these recent studies have raised the question whether early in the olfactory system, in addition to information on odor stimulus, changes in activity of mitral and tufted cells (MTs) could contain information relevant to decision making. Thus, even though anesthetized preparations can be incredibly informative, it is critical to study neuronal responses in awake and behaving animals exposed to different behavioral paradigms. This scenario will truly uncover the neuronal firing pattern/behavioral output relationship. In this chapter, we discuss the interesting current attempts to break the olfactory code signal processing in awake preparations. We discuss how changes in neuronal activity are related to olfactory stimulus and how they can be affected by experience and sniffing of odors. We also describe the relevance of temporal coding in the transmission of information about the odor identity (what is the smell?) and odor value (is the odor rewarded?). We emphasize recent studies in the OB and include related studies in other brain areas such as the piriform cortex (PC).
Section snippets
Odors Induce Substantial Glomerular Activity with Differential Timing of Activation as Input to the OB
Information on odor quality and intensity is conveyed in the awake or anesthetized animal through changes in neuronal activity in the glomerular layer (GL) of the OB (Wachowiak and Shipley, 2006). Of approximately 1000 olfactory receptors, olfactory sensory neurons (OSNs) expressing the same receptor convey their axons to one or two glomeruli in the OB (Mombaerts, 2006, Mombaerts et al., 1996, Serizawa et al., 2000). While the majority of OSNs are narrowly tuned, some neurons are quite
Odors Induce Substantial Changes in Mitral Cell Firing Rate in the Anesthetized Animal
After information about the odor cue is represented in the GL, it is transmitted to MTs whose changes in neuronal activity elicited by the glomerular input are modulated by local interneurons, such as periglomerular interneurons and granule cells (GCs) (Isaacson and Strowbridge, 1998, Jahr and Nicoll, 1982b, Schoppa et al., 1998, Wachowiak and Shipley, 2006). Olfactory signals processed by these local circuits are modified and transferred to the PC and other subcortical regions (Linster and
Odor-Induced Firing of Mitral Cells is High in Anesthetized Animals and Substantially Decreased in Awake Animals Because of Increased Inhibition by GCs
As opposed to MT responses in anesthetized preparations, in the awake animal odors elicit spared increases in firing rate (Cury and Uchida, 2010, Doucette and Restrepo, 2008, Doucette et al., 2011, Gschwend et al., 2012, Rinberg et al., 2006, Smear et al., 2011, Spors et al., 2012; Fig. 1). What can be influencing MT responses in the awake animal? The OB regulates MT neuronal activity and the transmission of information through inhibitory neurons by either the glomerular interneurons or GCs.
There is a Lack of Overall Odor-Induced Changes in Firing Rate in Mitral Cells in a Subset of Awake Animals
As stated above, sensory information processing is strikingly different in the awake state. Animals under anesthesia do not actively regulate stimulus sampling through changes in sniffing, a behavior that has been well documented in awake rodents and involves an increase in sniffing frequency while the animal is actively discriminating an odor (Carey et al., 2009, Doucette et al., 2011, Gire et al., 2013, Wachowiak, 2010). Moreover, under anesthesia, projections to the OB from other brain
Neural Representation of Input to OB Can Be Shaped by Sniff
Olfactory sampling can be actively modified by changes in respiration frequency. This active control on incoming sensory information allows animals to generate critical context-dependent odorant representations. Interestingly, activation of OSNs and concomitant input transmission to the GL can occur during the sniff even in the absence of an odor, suggesting that sniff itself could somehow activate OSNs. It has been proposed that this sniff-mediated effect is likely mediated by mechanical
Sniff-Locked MTs Firing Provides Odor Information
The MT cells are the main output from the OB to higher olfactory centers, such as PC and anterior olfactory nuclei. They convey odor information that has been represented and processed by local neural circuits in OB. The fact that spontaneous activity without odor stimulation and/or odor-evoked responses of most MT cells showed highly specific phase locking to sniffing cycle (Kepecs et al., 2006, Wachowiak, 2011) indicates profound and dramatic effects of sniff on the output neural activity in
Sniff and Local Field Potentials
While spikes encode information transmitted by single neurons, local field potential (LFP) recordings provide reliable information on synchronized activity of large groups of neurons (Buzsaki and Watson, 2012). Importantly, LFP oscillation in the OB transfers information on MT synchronization that is particularly important for olfactory-mediated tasks, such as olfactory discrimination (Beshel et al., 2007, Doucette et al., 2011, Kay, 2005, Lagier et al., 2007).
When an animal is engaged in
Sniff and Olfactory Afterimage
During behavior, animals can percept the odorant within a single sniff, and the responses of some MT cells are robust within the first sniff cycle (Cury and Uchida, 2010, Shusterman et al., 2011). However, in awake mice, some MT cells showed persistent responses to odors after the first sniff (Doucette and Restrepo, 2008, Doucette et al., 2011, Patterson et al., 2013), and responses after the first sniff were related to behavioral responses (Doucette and Restrepo, 2008, Doucette et al., 2011).
Conclusion
The awake behaving recording from mice has mushroomed in the last decade, resulting in a substantial increase of the understanding of the involvement of the OB in conveying information on the fact that odor identity and odor value are both present in MT activity. Likely, the information on odor identity is conveyed by the sniff-locked MT activity, while the information on odor value is conveyed by odor-induced changes in average MT rate. However, in future work, it is key to perform awake
Acknowledgments
Funded by NIH/NIDCD Grants R01 DC00566 and P30 DC04657 and National Natural Science Foundation of China (NSFC, 31100799).
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These authors contributed equally to this work.