Internal representation and memory formation of odor preference based on oscillatory activities in a terrestrial slug

Abstract

The terrestrial slug Limax exhibits a highly developed ability to learn odors with a small nervous system. When a fluorescent dye, Lucifer Yellow (LY), is injected into the slug's body cavity after odor -taste associative conditioning, a group of neurons in the procerebral (PC) lobe, an olfactory center of the slug, is labeled by LY. We examined the relationships between conditioning strategies and LY labeling. The positions of LY-labeled neurons in the PC lobe after appetitive conditioning were more apical than those after aversive conditioning and did not depend on the conditioned odor, suggesting that the biological value of odors affected the position of LY-labeled neural clusters. A simple computational model consisting of two layers of oscillators with electrical synaptic interaction was constructed based on physiological features of the PC lobe, and showed that the oscillatory phase difference between the layers contributed to determination of the positions of LY-labeled neurons, suggesting that phase difference in oscillatory activity plays a role in the association of odors and the preference for them. (Wehr and Laurent 1996); and (6) they play roles in the mechanisms of fine odor discrimination (Stopfer et al. 1997;Teyke and Gelperin 1999).For terrestrial slugs, olfactory information is the most important means of recognizing the external world, and slugs exhibit various types of odor learning (Sahley et al. 1981(Sahley et al. , 1990Hopfield and Gelperin 1989;Suzuki et al. 1994). Slugs have two pairs of tentacles that sense odors via olfactory receptors at their tips. Odor information is transferred to the procerebral (PC) lobe, which is the lateral part of the cerebral ganglion and is specialized for olfactory information processing in terrestrial slugs and snails (Ratte and Chase 1997;Chase 2000;Zaitseva 2000). On the surface of the PC lobe, large numbers of cell bodies of interneurons are arranged and elongate their neuropils toward the inside of the PC lobe, where afferent fibers from the tentacles are projected (Kawahara et al. 1997). The PC exhibits oscillation of local field potentials (LFP) at 0.7 Hz (Gelperin and Tank 1990). It is thus suitable for study of the contribution of oscillation to information processing in a nervous system that features learning, and has been studied extensively (for reviews, see Gelperin 1999Gelperin , 2006Watanabe et al. 2008). For example, LFP oscillation is synchronized over the entire PC lobe, with wave propagation from apical to basal parts (Delany et al. 1994;Kawahara et al. 1997;Kimura et al. 1998c). The application of learned odors changes the frequency of the LFP oscillation (Kimura et al. 1998a;Inoue et al. 2006). In addition, when a fluorescent dye, Lucifer Yellow (LY), is injected into the body cavity after odor learning, some of the PC interneurons incorporate the dye (Kimura et al. 1998b;Gelperin 1999;Ermentrout et al. 2001). Since the incorporation of LY depends on conditioning treatment and the duration between conditioning and LY injection (Kimura...

Neural and molecular mechanisms of microcognition inLimax

“…Control experiments showed that PC lesioned slugs were not anosmic (Kasai et al 2006). These results strongly support evidence from optical (Kimura et al 1998b;Toda et al 2000), molecular, and activitydependent dye uptake studies (Kimura et al 1998c;Sekiguchi et al 2008), also indicating a selective role of the PC lobe in odor learning.…”

“…However, ablation of the PC lobe did not affect detection of odors, because the ablated slugs showed normal avoidance to the innately aversive odor of garlic. Lucifer yellow injected immediately after conditioning stained a cluster of neurons in the PC lobe (Kimura et al 1998c;Sekiguchi et al 2008). The staining was selectively observed in the PC of the conditioned animals and has been suggested to reflect elevated neural activity.…”

Chromatophore Activity during Natural Pattern Expression by the Squid Sepioteuthis lessoniana: Contributions of Miniature Oscillation

“…Meanwhile, the tone of the skin, which is regulated by the exact expansion size of chromatophores [9], [10], [11], [12], may be determined by synchronous performance within the motor neural oscillations because the expansion is produced by the total activity of a set of the motor neurons innervating the specific chromatophore. It has been reported that oscillator networks are utilized for simultaneous expression or integration of different modalities of information (e.g., [21], [22]). We expect that the chromatophore control system of the squid will provide a typical and important model for understanding how the CNS integrates different modal information using an oscillator network.…”

Olfactory Memory Storage and/or Retrieval Requires the Presence of the Exact Tentacle Used During Memory Acquisition in the Terrestrial SlugLimax

“…In fact, the PC exhibits a learned odor-specific change in the oscillatory frequency or amplitude of the spontaneous local field potential oscillation (Kimura et al, 1998a;Nikitin and Balaban, 2000;Inoue et al, 2006), and incorporation of Lucifer yellow dye into PC neurons specifically following odor-associative memory formation (Kimura et al, 1998b;Ermentrout et al, 2001;Sekiguchi et al, 2010). Future studies may reveal such discernible changes triggered in the TG by olfactory learning.…”