Myogenic activity and serotonergic inhibition in the chromatophore network of the squids, Dosidicus gigas (Family Ommastrephidae) and Doryteuthis opalescens (Family Loliginidae)

Abstract

Seemingly chaotic waves of spontaneous chromatophore activity occur in the ommastrephid squid in the living state and immediately after surgical disruption of all known inputs from the central nervous system. Similar activity is apparent in the loliginid, but only after chronic denervation of chromatophores for 5-7 days. Electrically stimulated, neurally driven activity in intact individuals of both species is blocked by tetrodotoxin (TTX), but TTX has no effect on spontaneous wave activity in either or denervated Spontaneous TTX-resistant activity of this sort is therefore likely myogenic, and such activity is eliminated in both preparations by serotonin (5-HT), a known inhibitor of chromatophore activity. Immunohistochemical techniques reveal that individual axons containing L-glutamate or 5-HT (and possibly both in a minority of processes) are associated with radial muscle fibers of chromatophores in intact individuals of both species, although the area of contact between both types of axons and muscle fibers is much smaller in Glutamatergic and serotonergic axons degenerate completely following denervation in Spontaneous waves of chromatophore activity in both species are thus associated with reduced (or no) serotonergic input in comparison to the situation in intact Such differences in the level of serotonergic inhibition are consistent with natural chromogenic behaviors in these species. Our findings also suggest that such activity might propagate via the branching distal ends of radial muscle fibers.

Networks of linked radial muscles could influence dynamic skin patterning of squid chromatophores

“…These new 3D anatomical considerations lend support to earlier suggestion, based primarily on light microscopy (Froesch‐Gaetzi & Froesch 1977; Rosen & Gilly 2017), that radial muscles contact each other in several cephalopod species. Additional anatomical data combined with neurophysiological and pharmacological experiments will be needed to fully assess their prevalence and functional physiology.…”

“…These newly described ultrastructural connections among radial muscles provide detailed anatomical support for previous published suggestions that, in squid skin, there may be local peripheral coordination of chromogenic expression among neighboring chromatophores, putatively based on direct muscle interactions (Girod, 1883; Sereni, 1930; Froesch‐Gaetzi & Froesch, 1977; Rosen & Gilly 2017).…”

“…Since radial muscles can be visualized using β-actin and phalloidin (see also Rosen & Gilly, 2017), it should be possible to derive largearea statistics of muscle-muscle proximity from analysis of systematically tiled high magnification 3D scans of fluorescently labeled tissue.…”

“…The possibility of some degree of local patterning control enabled by its underlying structural basis in cephalopod skin has long been of interest (e.g., Hofmann, 1907;Sereni, 1930;Froesch-Gaetzi & Froesch, 1977;Reed, 1995a;Packard, 1992Packard, , 2011Bell et al, 2013;Rosen & Gilly, 2017). Those studies, while suggestive, did not find compelling evidence that muscles of adjacent chromatophores are interconnected by their muscles in any functional manner.…”

The Current State of Cephalopod Science and Perspectives on the Most Critical Challenges Ahead From Three Early-Career Researchers

“…Some important research topics that have been pursued in the last two decades with the various methods described and proposed above are the motor control of posture and limbs, especially regarding the parallel processing necessary to control 8 or 10 appendages of coleoids (e.g., Sumbre et al, 2001 , 2005 , 2006 ; Zullo et al, 2009 ; Levy and Hochner, 2017 ), as well as neural control of body patterning ( Wardill et al, 2012 ; Rosen and Gilly, 2017 ) and texture ( Gonzalez-Bellido et al, 2018 ). Finally, the existence and role of sleep in cephalopods, which undergo periods of behavioral and physiological quiescence that strongly resembles sleep in vertebrates ( Mather, 2008 ; Meisel et al, 2011 ; Frank et al, 2012 ) is in our view a fascinating area of inquiry that could give insight into the phylogenetic origins and biological reasons for sleep in animals.…”