Multiple longitudinal tracts in the cephalopod arm sensorimotor system

Abstract

Octopuses have an incredibly rich behavioral repertoire, exhibiting complex motor acts that require the coordination of eight highly flexible arms, each with hundreds of suckers. These movements are controlled by an axial nerve cord (ANC), equivalent to the spinal cord, situated in the center of the arm musculature. The ANC has a cell body layer which forms a U-shape around its neuropil and is capped aborally, or opposite the sucker, by the cerebrobrachial tract (CBT), a massive fiber bundle known to interconnect the arms and the brain. In vertebrate spinal cords, in addition to the major fiber tracts that interconnect the brain and spinal cord, there are spinospinal connectives that coordinate complex motor behaviors across the appendages. Here, we asked with tract-tracing and immunohistochemistry, whether an octopus arms ANC might also have intrinsic longitudinal connections for coordinated arm and sucker movements. We found that the ANC neuropil is enriched in longitudinal fibers. These fibers form distinct tracts, two within the oral (sucker-side) neuropil and two in the aboral (brachial-side) neuropil. In addition, CBT itself demonstrates four major subtracts, and DiI labeling and dextran tracing suggests that (1) the CBT also carries arm-intrinsic longitudinal connections and (2) the CBT and the neuropil tracts can be subcategorized into those that primarily connect with the sucker and those that serve the arm musculature. We also examined the organization of fiber-tracts in the ANC of the arms and tentacles of two species of squid, establishing that an aboral, extra-neuropil tract is a shared feature across all cephalopod species studied. In addition, the squids also had an oral longitudinal tract, though its positioning and size varied with species and appendage. In sum, these findings describe the neural substrate for coordinating motor behaviors across the length of a cephalopod appendage.