Abstract
The acquisition of olfactory information and its early processing in mammals are modulated by brain states through sniffing behavior and neural feedback. We imaged the spatiotemporal pattern of odor-evoked activity in a population of output neurons (mitral/tufted cells, MTCs) in the olfactory bulb (OB) of head-restrained mice expressing a genetically-encoded calcium indicator. The temporal dynamics of MTC population activity were relatively simple in anesthetized animals, but were highly variable in awake animals. However, the apparently irregular activity in awake animals could be predicted well using sniff timing measured externally, or inferred through fluctuations in the global responses of MTC population even without explicit knowledge of sniff times. The overall spatial pattern of activity was conserved across states, but odor responses had a diffuse spatial component in anesthetized mice that was less prominent during wakefulness. Multi-photon microscopy indicated that MTC lateral dendrites were the likely source of spatially disperse responses in the anesthetized animal. Our data demonstrate that the temporal and spatial dynamics of MTCs can be significantly modulated by behavioral state, and that the ensemble activity of MTCs can provide information about sniff timing to downstream circuits to help decode odor responses.
Highlights
Volatile odorants are sensed in mammals by olfactory sensory neurons (OSNs), which converge on structures called glomeruli in the olfactory bulb (OB) (Mombaerts, 2006; Sakano, 2010; Murthy, 2011)
Our data demonstrate that the temporal and spatial dynamics of mitral/tufted cells (MTCs) can be significantly modulated by behavioral state, and that the ensemble activity of MTCs can provide information about sniff timing to downstream circuits to help decode odor responses
We used population imaging to find that the spatial patterns of odor-evoked activity on the dorsal surface were generally similar in anesthetized and awake animals, but with some differences due to infra-glomerular signals that can likely be attributed to MTC lateral dendrites
Summary
Volatile odorants are sensed in mammals by olfactory sensory neurons (OSNs), which converge on structures called glomeruli in the olfactory bulb (OB) (Mombaerts, 2006; Sakano, 2010; Murthy, 2011). Olfactory information is processed by an intricate circuit of neurons, including several classes of interneurons, and the processed output is carried by mitral/tufted cells (MTCs) to a variety of cortical structures (Shepherd et al, 2004; Mori and Sakano, 2011; Murthy, 2011; Wilson and Sullivan, 2011). The activity of MTCs is tightly modulated by sniffing, and odor-evoked changes in MTC spiking often are apparent only when examined in the context of sniffing, especially when animals are awake (Macrides and Chorover, 1972; Cury and Uchida, 2010; Shusterman et al, 2011). At least some of the changes observed in the activity of MTCs in awake animals comes from altered sniff parameters (Carey and Wachowiak, 2011), but additional effects due to topdown circuit modulation remain to be investigated. There is substantial feedback from olfactory cortical regions and midbrain neuromodulatory centers to the OB (Price and Powell, 1970; Davis and Macrides, 1981; Luskin and Price, 1983; Kay and Laurent, 1999; Matsutani and Yamamoto, 2008), which are likely to be modulated in a state-dependent manner
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