Molluscan Memory of Injury: Evolutionary Insights into Chronic Pain and Neurological Disorders

Abstract

displays many functional similarities to alterations in mammalian nociceptors associated with the clinical problem of chronic pain. Moreover, in Aplysia and mammals the same cell signaling pathways trigger persistent enhancement of excitability and synaptic transmission following noxious stimulation, and these highly conserved pathways are also used to induce memory traces in neural circuits of diverse species. This functional and molecular overlap in distantly related lineages and neuronal types supports the proposal that fundamental plasticity mechanisms important for memory, chronic pain, and other lasting alterations evolved from adaptive responses to peripheral injury in the earliest neurons. Molluscan preparations should become increasingly useful for comparative studies across phyla that can provide insight into cellular functions of clinically important genes.

Peripheral injury induces long-term sensitization of defensive responses to visual and tactile stimuli in the squid Loligo pealeii, Lesueur 1821

“…cutaneous sensory neurons similar to those described in Aplysia and mammals (see Walters and Moroz, 2009), and (2) priming of defensive response systems so that specific motor patterns (inking, jetting) are triggered more readily by diverse stimuli, including visual stimuli, after injury (Erickson and Walters, 1988;Walters, 1994).…”

“…Aplysia californica (Kandel, 2001); Hirudo medicinalis (Sahley, 1995)] but only rarely with respect to its function or putative adaptive significance (but see Walters et al, 2001). Some cellular and molecular mechanisms of nociceptive sensitization are highly conserved among both invertebrates and vertebrates (Walters, 1994;Walters and Moroz, 2009); however, little is known about the incidence of nociceptive sensitization across different taxa and the extent to which behavioral patterns of sensitization vary across organisms with diverse lifestyles and different degrees of neural complexity.…”

The oyster genome reveals stress adaptation and complexity of shell formation

“…Molluscs have vital roles in the functioning of marine, freshwater and terrestrial ecosystems, and have had major effects on humans, primarily as food sources but also as sources of dyes, decorative pearls and shells, vectors of parasites, and biofouling or destructive agents. Many molluscs are important fishery and aquaculture species, as well as models for studying neurobiology, biomineralization, ocean acidification and adaptation to coastal environments under climate change 2,3 . As the most speciose member of the Lophotrochozoa, phylum Mollusca is central to our understanding of the biology and evolution of this superphylum of protostomes.…”

Pain in aquatic animals

“…Aplysia has nine central ganglia innervating some 10,000 neurons with cell bodies in peripheral nerve nets (Cash and Carew, 1989), so has a relatively simple CNS. The nociceptors found in Aplysia exhibit comparable electrophysiological properties to those of mammals (Illich and Walters, 1997;Walters and Moroz, 2009), and noxious stimulations results in reflex withdrawal of the gill, siphon, tail and head, and ink ejection (Kandel, 2001;. Indeed, damage to tissues and subsequent stimulation result in sensitization of Aplysia nociceptors and enhanced withdrawal reflex responses.…”