Identification of CO₂Chemoreceptors inHelix pomatia

Abstract

SYNOPSIS. Gas exchange in pulmonate snails of the family Helicidae occurs through a highly vascularized diffusion lung known as the mantle. The extent of ventilation of the mantle depends upon the duration and size of opening of an occlusible pore known as the pneumostome. In Helix aspersa and Helix pomatia, pneumostomal size and frequency of opening are exquisitely sensitive to CO 2 . Respiratory CO 2 chemosensitivity resides in a discrete region of the subesophageal ganglia. The discharge pattern of many neurons in the chemoreceptor area changes during stimulation with CO 2 . However, the electrophysiological response to CO, stimulation alone does not discriminate between CO 2 chemoreceptor cells and CO 2 -insensitive neurons active in the pneumostomal response to CO 2 . We identified a subset of CO 2 -sensitive neurons from the larger population of neurons active during CO 2 stimulation. The action potential discharge frequency of CO 2 chemosensory neurons increased in response to CO 2 stimulation. An increased discharge frequency of CO 2 -sensitive neurons was associated with increased pneumostomal opening, and both the size and the frequency of pneumostomal opening increased during CO 2 stimulation. Injecting depolarizing current into individual chemosensory neurons elicited opening of the pneumostome in the absence of CO 2 . Action potential generation in response to CO 2 was independent of synaptic transmission. Removal of individual CO 2 -sensitive cells or inhibition of action potential generation in CO 2 -sensitive cells reduced or eliminated pneumostomal responses to CO 2 . CO 2 sensitivity in chemoreceptor cells required extracellular calcium, but not sodium. Substituting barium for calcium supported chemoreceptor activity. In summary, we have identified respiratory related, chemosensory neurons that are CO 2 sensitive in the absence of synaptic input.

Multiple targets of chemosensitive signaling in locus coeruleus neurons: role of K+ and Ca2+channels

“…We believe that activation of Ca 2ϩ channels may be directly involved in the chemosensitive response to HA and IH. First, Ca 2ϩ channel activation has been implicated in chemosensitive signaling in invertebrate neurons (23,24). Second, HA-induced increased firing rate is only partially inhibited (Figs.…”

“…Another possibility exists. It has been shown in at least one invertebrate preparation, the terrestrial snail, that chemosensitive neurons respond to hypercapnia by activating Ca 2ϩ channels (23,24). If this is a general feature of the chemosensitive response of invertebrate neurons, and K ϩ channels are not largely involved, the activation of Ca 2ϩ channels by chemosensitive signals seen in LC neurons in the current study could represent a vestigial "invertebrate mechanism" with a "vertebrate mechanism," involving K ϩ channel inhibition and Na ϩ channel activation, superimposed.…”

“…In peripheral chemosensitive cells, changes of pH i and pH o resulted in inhibition of both K Ca channels, as well as of the TWIK-related acid-sensitive K ϩ (TASK) channel (7,8,10). Finally, during hypercapnia, Ca 2ϩ channels are activated in peripheral chemosensi-tive cells (9,47,48,67) and in invertebrate central chemosensitive neurons (24). Therefore, possible channel targets of chemosensitive signals include K ir , K Ca , TASK, and Ca 2ϩ channels.…”

Carbon dioxide sensitivity and its role in multifunctional neurons in the mollusk Onchidium

“…In order to show this behavior, coordination between the neurons that control the mantle would be necessary. Besides the Ip-1/2 neurons, it is hypothesized that a large number of CO 2 -sensitive neurons exist in the central ganglia, as noted in Helix (Erlichman and Leiter, 1997) or Aplysia (Brown and Berman, 1970), and that they work cooperatively to perform ventilatory behavior in Onchidium.…”

“…There are many CO 2 -sensitive neurons in the central ganglia of Helix, for which focal stimulation with CO 2 causes increased ventilation. Both mechanisms of increasing ventilation are reminiscent of the central control of respiration in vertebrates (Erlichman and Leiter, 1997;Putnam et al, 2004).…”