Motor neuronal control of tail-directed and head-directed siphon responses in Aplysia californica

Abstract

1. Cutaneous stimulation of opposite ends of the body causes qualitatively different siphon responses: tail stimulation causes flaring and backward bending (the siphon T response), whereas head stimulation causes constriction and slight anterior bending (the siphon H response). This paper characterizes the motor neuronal control of siphon T and siphon H responses. 2. The siphon response to tail nerve (p9) shock in a semi-intact preparation was indistinguishable from the siphon T response in intact or parapodectomized animals. Similarly, the siphon response to head nerve (c2) shock in this preparation was indistinguishable from the siphon H response in intact or parapodectomized animals. 3. Central siphon motor neurons (SMNs) were found to cause a wider variety of movements than previously reported. The movements produced by the LFSB cells strongly resemble the flaring response of the siphon to tail or tail nerve stimulation. The movements produced by RDS and LDS1 resemble components of the constricting response of the siphon to head or head nerve stimulation. 4. Among central SMNs, the LFSB cells show the strongest activation by posterior stimulation, whereas RDS and LDS1 show the strongest activation by anterior stimulation. The LFSA cells, which produce much weaker siphon constriction, are only activated slightly by posterior stimulation and are inhibited by anterior stimulation. Peripheral SMNs are inhibited by stimulation of head and tail nerves, and thus their activity does not directly contribute to siphon T and H responses. 5. Artificially activating central SMNs with the pattern of activity previously exhibited after tail or head nerve stimulation indicated the sufficiency of the LFSB cells for the siphon T response, and of RDS and LDS1 for the siphon H response. 6. Dramatic behavioral deficits produced by hyperpolarizing the LFSB cells during tail nerve stimulation, or by hyperpolarizing RDS and LDS1 during head nerve stimulation, indicated the necessity of these cells for the expression of directed siphon responses to tail or head stimulation, respectively. 7. Because of their apparent necessity and sufficiency for directional siphon responses to anterior and posterior stimulation, these few cells provide well-defined vantage points for studying neural mechanisms underlying the motor control and transformation of siphon responses. The four LFSB cells offer a special advantage for cellular analysis because they form a homogeneous functional unit in which any sampled LFSB cell can be used as a precise monitor of the total motor output underlying the siphon T response.(ABSTRACT TRUNCATED AT 400 WORDS)

Regulation of Behavioral and Synaptic Plasticity by Serotonin Release within Local Modulatory Fields in the CNS ofAplysia

“…The siphon LFS MNs also tended to fire somewhat more action potentials in response to tail-nerve shock than head-nerve shock (Fig. 4 A, B), in agreement with the behavior of intact animals, in which tail shock typically produces a flaring siphon response involving LFSs, whereas head shock produces a constricting response that is thought to rely on other subtypes of siphon MNs (LBS and RDS subtypes) (Hickie and Walters, 1995). In agreement with previous studies (Fang and Clark, 1996), L29 -LFS synapses were facilitated in response to tail-nerve shock (ϩ43 Ϯ 8%; n ϭ 6; p Ͻ 0.01).…”

Synaptic Facilitation and Behavioral Dishabituation in Aplysia: Dependence on Release of Ca2+ from Postsynaptic Intracellular Stores, Postsynaptic Exocytosis, and Modulation of Postsynaptic AMPA Receptor Efficacy

“…Sensorimotor cocultures, each comprising a single presynaptic sensory neuron and a single postsynaptic motor neuron, were fabricated using small siphon (LFS) motor neurons (Frost et al, 1988;Hickie and Walters, 1995) and pleural sensory neurons (Walters et al, 1983a). The neurons were dissociated from Aplysia (60 -100 g; Alacrity Marine Biological) and cultured as described previously (Lin and Glanzman, 1994a).…”

Heterosynaptic Facilitation of Tail Sensory Neuron Synaptic Transmission during Habituation in Tail-Induced Tail and Siphon Withdrawal Reflexes ofAplysia

“…LFS B siphon motor neurons were identified by their characteristic position on the ventral surface of the abdominal ganglion, by their ability to generate a specific tailward movement of the siphon when depolarized by intracellular current injection, and by their vigorous firing in response to tactile tail stimulation delivered to either side of the tail (Frost et al, 1988;Hickie and Walters, 1995). Tail motor neurons were identified on the basis of their location in the pedal ganglia, their size, and their characteristic firing patterns, both spontaneous and in response to tail stimuli (Walters et al, 1983).…”