Parasite-induced alterations of sensorimotor pathways in gammarids: collateral damage of neuroinflammation?

Investigating candidate neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects

“…Neuromodulatory systems, in particular biogenic amines, opioids and the diffusible gaseous signalling molecule NO, are thus considered as potential targets of manipulative parasites (Kavaliers et al, 2000;Adamo, 2002;Helluy and Thomas, 2003;Adamo, 2013;Helluy, 2013). More specifically, the tight connection between the immune system and the nervous system could provide parasites with an indirect and less expensive method of altering host behaviour.…”

“…More specifically, the tight connection between the immune system and the nervous system could provide parasites with an indirect and less expensive method of altering host behaviour. From the initial ability to counter the host's immune system, parasites would have secondarily evolved the ability to subvert the bi-directional immune-brain circuitry, eventually modulating sensory-motor processing pathways, in particular those underlying cue-oriented behaviour that facilitate trophic transmission (Adamo, 2002;Adamo, 2013;Helluy and Thomas, 2003;Helluy, 2013;Lafferty and Shaw, 2013).…”

“…This is particularly relevant to manipulative parasites, which alter the habitat choice and defensive behaviour of their hosts in ways that potentially increase their own transmission efficiency (Lafferty and Shaw, 2013). Investigation of the mechanisms underlying parasitic manipulation suggests that alteration of the host's neuromodulatory system is a common feature of manipulated hosts (Thompson and Kavaliers, 1994;Adamo, 2002;Adamo, 2013;Helluy, 2013;Lafferty and Shaw, 2013). Indeed, several studies involving both vertebrate and invertebrate hosts have reported altered levels of neuromodulators or neuropeptides concomitant with a parasite-induced change in behaviour (see references in Table1), or changes in expression of genes or proteins linked to biogenic amine metabolism in the brain (Hoek et al, 1997;Biron et al, 2005;Ponton et al, 2006;Prandovszky et al, 2011;Biron, 2013).…”

“…(2) A parsimonious functional argument, based on the intimate connection between the immune, endocrine and neural systems, and the life-long plasticity of the host's neuromodulatory network (Benton et al, 1997;Harzsch et al, 1999;Adamo, 2002;Beltz and Sandeman, 2003;Maier, 2003). According to the psychoneuroimmune hypothesis of parasitic manipulation (Adamo, 2002;Helluy, 2013), these properties of the neural and immune systems have probably been hijacked by parasites with the ultimate consequence of increasing their transmission. (3) A parsimonious evolutionary argument, considering that the phylogenetic conservatism of neuromodulatory, signalling and immune systems may facilitate a molecular cross-talk between the parasite and the host (Salzet et al, 2000;Maier 2003;Caveney et al, 2006).…”

Toxoplasma gondii infection and behaviour – location, location, location?

“…Classic examples include those involving the alteration of host behaviour as a means to increase transmission of the parasite, such as that of the trematode Dicrocoelium dendriticum, which induces infected ants to 'freeze' at the top of a blade of grass at dusk, enhancing their consumption by grazing ruminants, or another trematode, Euhaplorchis californiensis, which alters the behaviour of the California killifish, increasing the likelihood of its consumption by birds, the parasite's definitive host (Moore, 2013;Lafferty and Shaw, 2013). Another example is the amphipod Gammarus, which becomes attracted to light when infected with Polymorphus paradoxus, an Acanthocephalan, increasing consumption by the parasite's definitive vertebrate host (Helluy, 2013). Understanding these alterations is complicated by the fact that each parasite exerts multiple effects on it host that may result from multiple parasite mechanisms (Cézilly et al, 2013).…”