Mechanosensory Neurons InnervatingAplysiaSiphon Encode Noxious Stimuli and Display Nociceptive Sensitization

Abstract

Numerous studies of learning and memory in Aplysia have focused on primary mechanosensory neurons innervating the siphon and having their somata in the left E (LE) cluster of the abdominal ganglion. Although systematic analyses have been made of the responses of these LE cells to mechanical stimulation of the tightly pinned siphon, little is known about corresponding responses when the siphon is unrestrained. The present study demonstrates that LE mechanosensory thresholds in the freely moving siphon are much higher than in the pinned siphon. Light tactile stimuli adequate to activate central neurons and reflexive siphon movements often fail to activate the LE cells when the siphon is unrestrained. Because the LE cells display increasing discharge to increasing pressures, with maximal activation by crushing or tearing stimuli that cause tissue injury, they satisfy accepted definitions of nociceptor. Indeed, they show similarities to vertebrate Adelta nociceptors, including a property apparently unique (among primary afferents) to nociceptors-sensitization by noxious stimulation of their receptive field. Either pinching or pinning the siphon decreases LE cell mechanosensory threshold and enhances soma excitability. Such stimuli reduce effective tissue compliance and cause neuromodulation that enhances sensory responsiveness. These results, and recent descriptions of predatory attacks on Aplysia, suggest that LE sensory neurons are tuned to grasping and crushing stimuli that threaten or produce bodily harm. LE cell sensitization has effects, resembling hyperalgesia and allodynia, that compensate for loss of sensory function during injury and help protect against subsequent threats.

Perceptual Correlates of Nociceptive Long-Term Potentiation and Long-Term Depression in Humans

“…It may not be surprising that longterm memory in the human injury-detection system is found to be related to the highly conserved mechanism of learning (LTP), considering the fact that during evolution, strong injury-related selection pressures have shaped the nervous systems of all species (Walters, 1994). Research in many areas of neuroscience uses experimental paradigms that simulate aspects of actual or threatened injury to study mechanisms of learning and memory (e.g., conditioning of the gill withdrawal reflex in Aplysia) (Illich and Walters, 1997;Kandel, 2001). Our data show that neurogenic hyperalgesia, which is an aspect of injury-related behavior in humans, shares characteristics with both homosynaptic and heterosynaptic types of LTP.…”

Changes in the nitric oxide system in the shore crab Hemigrapsus sanguineus (Crustacea, decapoda) CNS induced by a nociceptive stimulus

“…It has been shown in crustaceans that the NO-ergic nerve fibers of sensory neuropils originate from the sensory neurons of peripheral tissues (Ott et al, 2007). Their physiology is similar to mammalian low-threshold mechanoreceptors (Byrne et al, 1974) or typical nociceptors (Illich and Walters, 1997) and their noxious-induced responses has been characterized in some invertebrate species (Shen et al, 2002), including crustaceans Barr et al, 2007;Elwood and Appel, 2009;Puri and Faulkes, 2010). In the sensory neuropils, fibers from cheliped receptors make synaptic contacts with dendrites of interneurons and motoneurons (Elson, 1996;Mulloney et al, 2003).…”

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

“…In the modulatory field that we studied in the abdominal ganglion, siphon SNs (LEs) lie in close proximity to the siphon MNs (Fig. 9B1) (Frost and Kandel, 1995;Illich and Walters, 1997). In this area, 5-HT release was maximal after siphon-nerve shock, which activates LE siphon SNs.…”