Elsevier

Biosystems

Volume 103, Issue 3, March 2011, Pages 348-354
Biosystems

Offset response of the olfactory projection neurons in the moth antennal lobe

https://doi.org/10.1016/j.biosystems.2010.11.007Get rights and content

Abstract

We investigated a population activity of central olfactory neurons after the termination of odor input. Olfactory response of projection neurons in the moth primary olfactory center was characterized using in vivo intracellular recording and staining techniques. The population activity changed rapidly to the different states after the stimulus offset. The response after stimulus offset represents information regarding odor identity. We analyzed the spatial distribution of offset-activated glomeruli in a virtual neuronal population that was reconstructed using accumulated individual recordings obtained from different specimens. The offset-activated glomeruli tended to be widely distributed, whereas the onset-activated glomeruli were relatively clustered. These results suggest the importance of lateral interaction in shaping the offset olfactory response.

Introduction

Insect olfactory systems are useful models for analyzing sensory information processing because they are relatively simple (Hildebrand and Shepherd, 1997) and have clear anatomical landmarks, which facilitate the integration of data obtained from different experiments. Odorants are detected by the olfactory receptor neurons on the antennae and translated into electrical signals. These signals are processed in the antennal lobe, which is the primary olfactory center in the insect brain (Schachtner et al., 2005). The antennal lobe is composed of glomeruli, the functional units of the olfactory system, and is important in temporal integration and gain control (Lemon and Getz, 2000, Olsen et al., 2010). Local interneurons connect glomeruli and are hypothesized to be important for the processing in the antennal lobe. The processed information is carried by projection neurons (PNs), which are the functional analog of mitral cells in mammalian olfactory bulb, and sent to the protocerebrum, where multimodal sensory information are integrated.

Odor response properties of PNs have been widely investigated by the use of electrophysiology and optical imaging. Olfactory information is encoded by spatially and temporally organized activity of the PNs in the antennal lobe (Stopfer et al., 2003, Lei et al., 2004, Daly et al., 2004). The response of the PNs is dynamic, whereas the response of olfactory receptor neurons is relatively stable. The activity pattern changes with time during odor presentation (Mazor and Laurent, 2005). The process is thought to be important for decorrelation of similar odors (Friedrich and Laurent, 2001). PNs also show activity after the termination of odor input (Kanzaki et al., 1989, Sachse and Galizia, 2002, Brown et al., 2005, Mazor and Laurent, 2005, Silbering et al., 2008). Although there are many studies about the activity of PNs during odor presentation, the response after the termination of odor presentation has not yet been focused thus far. The researches that systematically analyze offset responses are very few (Kashiwayanagi et al., 1994, Sachse and Galizia, 2002). The computational role of offset responses pertaining to other sensory modalities has been revealed (Liang et al., 2008, Pei et al., 2009, Takahashi et al., 2004), and it is possible that the offset response might have several functions in olfactory processing.

Here we analyzed the offset olfactory response of PNs in the antennal lobe of the silkmoth Bombyx mori and examined whether odor discrimination can also be accomplished by the response of PNs after stimulus offset. In the silkmoth, we have previously described odor representation of PN during odor presentation (Namiki and Kanzaki, 2008). Odor representation by a population of PNs was spatially and temporally organized. We found that the response of PNs often sustained after the stimulus offset. In the present study, we especially focused on the response after the termination of odor stimulus and investigated their function and mechanisms by analyzing the population activity.

Section snippets

Intracellular recording and staining

We used the method described in our previous study (Namiki and Kanzaki, 2008, Namiki et al., 2008). We used the silkmoth B. mori (Lepidoptera: Bombycidae). Male silkmoths were reared at 26 °C and 60% relative humidity and fed an artificial diet. Each moth was fixed in a plastic chamber, and its head was immobilized using a notched plastic yoke slipped between the head and thorax. The brain was exposed by opening the head capsule and removing the large tracheae; the intracranial muscles were

Results

We investigated the offset response of PNs in the moth antennal lobe at a population level. Individual PNs had dendritic processes within the glomeruli and sent axonal projection to the higher order center (Fig. 1A). By monitoring the response of this neuronal population, we examined the representation of plant odors after the stimulus offset. We then examined whether the offset response could encode odor identity. We finally analyzed the spatial pattern of the offset response to reveal the

Discussion

In the present study, we characterized the response patterns of PNs in the moth antennal lobe after the termination of odor input. Odor representation by a population of PNs rapidly moved to the different states (Fig. 1, Fig. 3). At a population level, the offset response pattern had the ability to encode information regarding odor identity (Fig. 2). The patterns were not correlated with the response pattern during odor presentation (Fig. 3) and were spatially distributed (Fig. 4). We discuss

Acknowledgements

This research was supported by Research and Development of the Next-Generation Integrated Simulation of Living Matter, a part of the Development and Use of the Next-Generation Supercomputer Project, a grant from a Grant-in-Aid for Scientific Research (B) (18370028) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan, and Sasagawa Research Grant from the Japan Science Society.

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