Elsevier

Brain Research

Volume 896, Issues 1–2, 30 March 2001, Pages 30-35
Brain Research

Research report
Modulation of oscillatory neural activities by cholinergic activation of interneurons in the olfactory center of a terrestrial slug

https://doi.org/10.1016/S0006-8993(00)03242-XGet rights and content

Abstract

The neurons in the procerebrum (PC) of the terrestrial slug Limax marginatus show regular oscillation of their membrane potential, and the oscillation has been implicated in olfactory processing. The neural mechanisms for the generation and modulation of the oscillation have been poorly understood. In the present work, we examined the ionic conductances evoked by acetylcholine (ACh) in the PC neurons and the effects of ACh application on the population activities of intrinsic and extrinsic neurons. The PC neurons are categorized into bursting neurons, which are putative local inhibitory neurons, and nonbursting neurons, which likely mediate the input and output of information in the PC. Bath application of ACh augmented the local field potential oscillation in the PC. Perforated patch recording from single PC neurons revealed that ACh has direct excitatory effects on bursting neurons, while it suppresses the activity of nonbursting neurons, possibly via augmented inhibitory synaptic input from bursting neurons. The correlation between the membrane potential of bursting neurons and the frequency of oscillation suggests that bursting neurons are the main determinant of the oscillation frequency. Application of ACh also resulted in a reduction of the oscillation amplitude in the olfactory nerve, suggesting that the frequency modulation in the oscillatory network could change the activities in the follower neurons.

Introduction

The olfactory centers of a wide variety of animals show synchronized oscillatory activities [1], [6], [19]. The procerebrum (PC) of the terrestrial slug Limax is comprised of about 105 neurons, and these neurons also show a synchronized oscillation of the membrane potential [7], [16]. The isolated brain preparation of Limax has the advantage that it allows direct observation and manipulation of neural activities without disruption of the network and the input/output pathways. The examination of the neural activities in the Limax PC thus far has revealed that the oscillation of the PC neurons is highly regular and observed without any afferent input [7], and is modulated when an odor is delivered to the olfactory receptors in a manner that is dependent on the quality and value of the odorant [13], [17]. However, two major problems about the neural oscillation have yet to be solved: one is how the oscillation is generated and controlled in the network, and the other is what roles the oscillation could have for information processing.

Recent researches using patch clamp recording from single PC neurons have reveled the existence of two types of neurons in the PC: bursting and nonbursting neurons [18]. Morphological [25] and electrophysiological [14], [18] studies have suggested that the bursting neurons are local inhibitory interneurons, whereas the nonbursting neurons make connections with extrinsic neurons. Synchronized bursting in bursting neurons is thought to evoke inhibitory postsynaptic potentials (IPSPs) in the nonbursting neurons, and the IPSPs result in the oscillatory local field potential (LFP), which is recorded from the surface of the PC [18]. There is increasing evidence for the existence of various neurotransmitters and receptors in the PC [8], [11]. Especially, fast acting transmitters which have effects within the order of milliseconds are thought as essential for the synaptic interactions involved in the generation of oscillatory activities, and could be used to modulate the neural activity reversibly. Our previous work [26] focused on the actions of glutamate on the PC neurons, and suggested the possible involvement of glutamate as a transmitter in the PC. However, the action of glutamate on the PC neurons was mainly inhibitory, and the existence of an excitatory neurotransmitter has been predicted to explain the repetitive synchronized bursting in the bursting neurons. In fact, the bursting neurons show strong excitatory input, possibly from nonbursting neurons, which could underlie the odor input pathway [14]. Acetylcholine (ACh) is one such putative fast acting transmitter which is also widely distributed in molluscan nervous systems [24]. Therefore, we examined the effects of ACh on single PC neurons and their relationship to the network activity.

The information processed by the oscillating network should be transmitted to output neural systems. The molluscan preparations are also suitable for the studies of interactions between the central neural systems and the periphery because of their well-preserved structure and function in vitro. Therefore, we have also focused on the relationship between the PC neural activity and neurons receiving input form the PC, and examined the effects of central modulation on the peripheral neural activities.

Section snippets

Materials and methods

Recordings were made in an isolated cerebral ganglion of the slug Limax marginatus. Dissection and perforated patch recording of PC neurons were made essentially as described elsewhere [26]. The PC neurons are categorized into the two major types, the bursting and nonbursting neurons, and both of these neuron types are found throughout the PC. Therefore, we made random selection of neurons and checked the type of the neurons based on their firing patterns. The preparation was placed in a

Results

Bath-application of ACh to the cerebral ganglion augmented the frequency of the LFP oscillation of the PC (Fig. 1), as has been demonstrated previously [15]. The augmentation of frequency was accompanied by a reduction of the amplitude of the LFP events. These results indicate that the PC neurons possess ACh receptors that augment the oscillatory activity. We then examined the cellular mechanisms of ACh-induced augmentation of oscillation frequency with perforated patch recording in single PC

Discussion

The present work showed that: (1) ACh stimulates the bursting neurons and suppresses the nonbursting neurons; (2) ACh augments the synchronized oscillation; and (3) the augmented oscillatory activity also suppresses the activity of the neurons receiving an input from the PC neurons.

The correlation between the excitation of bursting neurons and the augmentation of the synchronized oscillatory activity of the PC suggests that the augmentation of the oscillatory activity by ACh is caused by

Acknowledgements

We thank Dr. H. Ooya for supplying the slugs. This work was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture, Japan (Nos. 11771408, 12048209 and 12307053) and by a grant from the Program for Promotion of Basic Research Activities for Innovative Biosciences, Japan.

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