Bottom-up and top-down modulation of early odor representations imaged in the behaving animal

University College Dublin (2009) Proc Physiol Soc 15, SA89

Research Symposium: Bottom-up and top-down modulation of early odor representations imaged in the behaving animal

M. Wachowiak1,2, R. M. Carey2, N. Pìrez1, D. W. Wesson1, J. V. Verhagen1

1. Biology, Boston University, Boston, Massachusetts, USA. 2. Biomedical Engineering, Boston University, Boston, Massachusetts, USA.

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Sensory processing is typically thought to act on representations of sensory stimuli that are relatively fixed at low levels and become increasingly complex and subject to modulation at higher levels in the nervous system. Here I present recent findings from our laboratory demonstrating that odor representations can be transformed at low levels – as early as the primary sensory neurons themselves – via a variety of different mechanisms in the behaving animal. In order to investigate this question, we have optical imaging with calcium-sensitive dyes or genetically encoded probes (e.g. synaptopHluorin) to monitor receptor neuron input to the olfactory in awake, head-fixed rats and mice performing olfactory discrimination tasks. Animals were headfixed via a skull screw chronically implanted under anaesthesia. These experiments revealed that odor representations at this level are temporally dynamics and tightly linked to odor sampling behavior (i.e. ‘sniffing’). During low-frequency sniffing, each inhalation of odorant elicits a burst of action potentials with a duration of ~100 ms and a relatively slow mean rise-time of 84 ± 40 (s.d.) ms, suggesting a progressive increase in ORN activation as odorant flows through the nasal cavity. These activation patterns are diverse but odorant-specific, with latencies and rise-times remaining uniform across successive inhalations of the same stimulus. Importantly, switching to high-frequency sniffing during active odor investigation can dramatically and rapidly alter the temporal structure and magnitude of sensory input. During high-frequency sniffing, the temporal coherence between ORN inputs and the respiratory cycle is strongly reduced, and overall input magnitudes are attenuated. This effect of this change is to shape – via bottom-up, receptor-driven mechanisms – which features of the olfactory landscape are emphasized and likely to alter how information is processed by the olfactory bulb network. At the same time, neural substrates exist for presynaptically modulating the strength of sensory input to the bulb as a function of behavioral state. We have found that increases in attention elicited by novel olfactory stimuli can modulate the strength of odor-evoked transmitter release from receptor neurons in awake mice. In vivo pharmacological experiments have provided evidence that the systems most likely to be involved in this modulation are cholinergic and serotonergic centrifugal inputs to the olfactory bulb glomerulus, which likely act by modulating the strength of GABA-mediated inhibition onto receptor neuron presynaptic terminals. Together, sniffing behavior and presynaptic inhibition have the potential to mediate – or at least contribute to – sensory processing phenomena such as figure-ground separation, intensity-invariance, and context-dependent and attentional modulation of response properties. Thus, ‘high-order’ processing can occur even before sensory neurons transmit information to the brain.



Where applicable, experiments conform with Society ethical requirements.

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