Investigation of burst generation by the electrically coupled cyberchron network in the snail Helisoma using a single‐electrode voltage clamp

Abstract

This paper describes the results of investigating burst generation by the cyberchron network in the snail Helisoma. The cyberchron network is composed of aproximately 20 electrically coupled neurons and controls the feeding behavior of the snail. The electrical coupling between network members has made it particularly difficult to distinguish between the importance and involvement of single-cell and network properties in burst generation by this system. The present investigations utilized the new single-electrode voltage clamp to examine the membrane properties and network interactions of the cyberchron neurons: (1) A slow outward current is activated by moderately large depolarizing commands (-40 to 0 mV) and does not undergo inactivation decay (i.e., decline in magnitude) during a command potential step maintained for 10 sec or more. The lack of inactivation of the outward current in cyberchron neurons appears to be due to the dominating role of a Ca-dependent K current. (2) There are two functionally distinct classes of cyberchrons--current generator cyberchrons and follower cyberchrons. (3) Primary current generator cyberchrons have membrane properties similar to endogenous bursting neurons (e.g., persistent inward Ca current and negative resistance region in I-V plot) and appear to provide the main driving and timing current for the rest of the network. (4) The vast majority of cyberchrons are secondary current generator cyberchrons with membrane properties which exhibit inward-going rectification and appear to burst as a result of regenerative excitation with one another and the primary current generator cyberchrons. (5) The second class of cyberchrons are driven by the electrical synaptic input from the current generator cyberchrons, do not exhibit inward-going rectification, and are called follower cyberchrons. (6) Burst termination is due to activation of a slow outward tail current in most cyberchrons during the burst (probably Ca-activated K current) which causes a hyperpolarization in individual cyberchrons, terminating the burst. (7) Decay of the outward tail current causes the cyberchrons to depolarize, which activates the persistent inward Ca current in the primary current generator cyberchrons, starting the burst cycle anew.

Impulse pattern generation in a crayfish abdominal postural motoneuron

“…Some examples include recurrent synaptic inhibition (Anderson et al 1964), slow cyclic potassium conductances (Junge and Stephens 1973), calcium activated potassium conductances (Merickel and Gray 1980), and electrogenic Na+/K + pumps (Sokolove and Cooke 1971;Jansen and Nicholls 1973). …”

The synaptic nature of the paroxysmal depolarizing shift in hippocampal neurons

“…A number of network-driven bursts have been described in the literature. The proposed mechanisms for these network-driven bursts have ranged from simple mutual inhibitory interactions (47, 60} to complex interactions of chemical and electrical synapses [19,20,30,31,45,50,54,611.…”

Contextual modulation of multifunctional central pattern generator

“…Previous work had indicated that different cells within the BAC network show differential coupling and variability in bursting patterns (Merickel and Gray, 1980). Some of them were classified as primary burst generators and others as secondary followers.…”

“…In the pulmonate snail Helisoma, a group of about 40 electrotonically coupled cells, termed 'cyberchron' neurons, were identified in the buccal ganglia (Kater, 1974;Kaneko et al, 1978Merickel and Gray, 1980). This cyberchron network [since renamed buccal A cluster cells (BACs) (Murphy, 2001;Murphy, 1991)] was initially thought to be the pattern generator but its function remains unclear.…”

“…The burst generation properties of this neural network have been studied using single-electrode voltage clamp techniques (Merickel and Gray, 1980) and computer simulation models . Although these experiments elegantly described the electrical properties of the cells, morphological characterizations of the BAC cells were not very clear because of a lack of good intracellular dyes at that time.…”