Respiratory behavior in the pond snail Lynmaea stagnalis

Abstract

Previously (Syed et al. 1991) we described the ventilatory behavior of the pond snail Lymnaea stagnalis and identified motor neurons that innervate various muscles involved in this behavior. In the present study we describe an interneuronal network that controls ventilatory behavior in Lymnaea. An identified interneuron, termed the input 3 interneuron (Ip.3.I), was found to be involved in the opening movement of the pneumostome (expiration), whereas another identified interneuron known as visceral dorsal 4 (V.D.4) caused its closure (inspiration). These cells have reciprocal inhibitory connections with each other, which accounts for their opposing effects on common follower motor neurons. In isolated brain preparations a third identified interneuron, right pedal dorsal 1 (R.Pe.D. 1) initiated the respiratory cycle by the excitation of Ip.3.I. Whereas Ip.3.I in turn excited R.Pe.D.1, the connections between R.Pe.D.1 and V.D.4 were mutually inhibitory. Both Ip.3.I and V.D.4 were active during spontaneously occurring respiratory behavior as recorded from semi-intact preparations, and selective hyperpolarization of V.D.4 during such spontaneous activity disrupted the respiratory behavior. Regarding peripheral feedback, the mechanical stimulation of the pneumostome during its opening movements not only caused closure but also inhibited Ip.3.I in the middle of its discharge. Ip.3.I and V.D.4 were also found to be multifunctional, inhibiting both locomotor and whole body withdrawal neural networks. We conclude from these results that the rhythmic patterned activity underlying respiratory behavior in Lymnaea is generated centrally, and that the network described here therefore comprises a central pattern generator.

Proceedings of the Physiological Society, 18‐19 December 1990, Birmingham Meeting: Communications

“…A pair of electrically coupled, identified neurones (L. and R.Pe.D. 11) lying in the pedal ganglia of the pond snail Lymnaea stagnalis (L.) appear to have synaptic actions on a number of neurones involved in control of the foot and body wall as well as neurones of the cardiorespiratory system (Syed, 1988;Syed & Winlow, 1988). Here we present evidence that some of these connections are electrical whilst others are chemical in nature.…”

Proceedings of the Physiological Society, 18‐19 December 1990, Birmingham Meeting: Communications

“…A pair of electrically coupled, identified neurones (L. and R.Pe.D. 11) lying in the pedal ganglia of the pond snail Lymnaea stagnalis (L.) appear to have synaptic actions on a number of neurones involved in control of the foot and body wall as well as neurones of the cardiorespiratory system (Syed, 1988;Syed & Winlow, 1988). Here we present evidence that some of these connections are electrical whilst others are chemical in nature.…”

Functional recovery of respiratory behavior during axonal regeneration in snails (Lymnaea stagnalis) is experience dependent.

“…There were no obvious differences in the number of stained neurons in the CNSs of snails, regardless of whether they were allowed to lung ventilate during the period of axonal regeneration. Moreover, anterograde staining with Lucifer Yellow of either the RPeD1 or the RPA (Syed et al, 1991; Syed & Winlow, 1991b) showed that these neurons had regenerated their axons by 5 weeks after axotomy. Figure 8B shows anterograde Lucifer Yellow staining of RPeD1 5 weeks after crush of the anal and right parietal nerves.…”

Dopaminergic Central Neurons and Peripheral Sensory Systems in Pteropod and Nudibranch Molluscs

“…Clearly, these giant dopaminergic neurons (∼200–300 µm) are homologous cells known to be involved in the control of respiratory behaviors as parts of the respiratory central pattern generator (Moroz 1990; Syed et al. 1990, 1991; Syed and Winlow 1991; Moroz and Winlow 1992; Winlow et al. 1992).…”

Proceedings of the Physiological Society, 18‐19 December 1990, Birmingham Meeting: Communications

“…A pair of electrically coupled, identified neurones (L. and R.Pe.D. 11) lying in the pedal ganglia of the pond snail Lymnaea stagnalis (L.) appear to have synaptic actions on a number of neurones involved in control of the foot and body wall as well as neurones of the cardiorespiratory system (Syed, 1988;Syed & Winlow, 1988). Here we present evidence that some of these connections are electrical whilst others are chemical in nature.…”

Functional recovery of respiratory behavior during axonal regeneration in snails (Lymnaea stagnalis) is experience dependent.

“…There were no obvious differences in the number of stained neurons in the CNSs of snails, regardless of whether they were allowed to lung ventilate during the period of axonal regeneration. Moreover, anterograde staining with Lucifer Yellow of either the RPeD1 or the RPA (Syed et al, 1991; Syed & Winlow, 1991b) showed that these neurons had regenerated their axons by 5 weeks after axotomy. Figure 8B shows anterograde Lucifer Yellow staining of RPeD1 5 weeks after crush of the anal and right parietal nerves.…”

Dopaminergic Central Neurons and Peripheral Sensory Systems in Pteropod and Nudibranch Molluscs

“…Clearly, these giant dopaminergic neurons (∼200–300 µm) are homologous cells known to be involved in the control of respiratory behaviors as parts of the respiratory central pattern generator (Moroz 1990; Syed et al. 1990, 1991; Syed and Winlow 1991; Moroz and Winlow 1992; Winlow et al. 1992).…”

Proceedings of the Physiological Society, 18‐19 December 1990, Birmingham Meeting: Communications

“…A pair of electrically coupled, identified neurones (L. and R.Pe.D. 11) lying in the pedal ganglia of the pond snail Lymnaea stagnalis (L.) appear to have synaptic actions on a number of neurones involved in control of the foot and body wall as well as neurones of the cardiorespiratory system (Syed, 1988;Syed & Winlow, 1988). Here we present evidence that some of these connections are electrical whilst others are chemical in nature.…”

Functional recovery of respiratory behavior during axonal regeneration in snails (Lymnaea stagnalis) is experience dependent.

“…There were no obvious differences in the number of stained neurons in the CNSs of snails, regardless of whether they were allowed to lung ventilate during the period of axonal regeneration. Moreover, anterograde staining with Lucifer Yellow of either the RPeD1 or the RPA (Syed et al, 1991; Syed & Winlow, 1991b) showed that these neurons had regenerated their axons by 5 weeks after axotomy. Figure 8B shows anterograde Lucifer Yellow staining of RPeD1 5 weeks after crush of the anal and right parietal nerves.…”

Dopaminergic Central Neurons and Peripheral Sensory Systems in Pteropod and Nudibranch Molluscs

“…Clearly, these giant dopaminergic neurons (∼200–300 µm) are homologous cells known to be involved in the control of respiratory behaviors as parts of the respiratory central pattern generator (Moroz 1990; Syed et al. 1990, 1991; Syed and Winlow 1991; Moroz and Winlow 1992; Winlow et al. 1992).…”