Proprioceptive hair cells on the neck of the squid Lolliguncula brevis :a sense organ in cephalopods for the control of head-to-body position

Abstract

Decapod cephalopods, such as cuttlefishes and squids, have a distinct neck region that allows movements (roll, pitch and yaw) of the head relative to the body. This paper describes the structure, innervation and central pathways of proprioceptive hair cells on the neck of the squid Lolliguncula brevis that sense such movements and control head-to-body position. These hair cells exist on the dorsal side of the neck underneath the nuchal cartilage, close to the animal’s midline on either side of the nuchal crest. On each side, the hair cells can be divided into an anterior and a posterior group of 25—35 and 70—80 cells, respectively. An individual hair cell carries up to 300 kinocilia of equal length (about 30 pm), arranged in up to seven rows. The hair cells of the left and right anterior group are morphologically polarized in the medial direction, whereas the hair cells of the left and right posterior group are polarized in the anterior direction. The hair cells are primary sensory cells. They are innervated by a branch of the postorbital nerve and project ipsilaterally into the ventral part of the ventral magnocellular lobe. Efferent synaptic contacts are present at the base of the hair cells. In behavioural tests the influence of the neck hair cells on head position control was investigated. During imposed body rolls, a unilateral deafferentation of the cells caused an asymmetric change of the compensatory head roll response and elicited a head roll offset to the operated side. Bilateral deafferentation of the cells elicited a downward head pitch offset. This offset was superimposed on the compensatory head pitch response during imposed body pitch. These morphological and behavioural findings show that the neck hair cells and the associated nuchal cartilage structures of Lolliguncula brevis form a neck receptor organ that, together with statocyst an visua inputs, controls the position of the animal’s head and body.