The mind and brain of an octopus: smart supercharged-snail.

Octopuses are masters of camouflage, solving complex tasks, and their cognitive ability is said to approach that of some small mammals. Since the late Cambrian period, octopuses have spread throughout all ocean habitats. Notably, the greatest diversity of octopus species is found in the Indo-Pacific coastal waters, where varied selection pressures have driven a wide range of adaptations. These include changes in life modes such as circadian rhythms (nocturnal vs diurnal), and habits (solitary vs partially social). Their sensory and nervous systems have thus evolved in fascinating ways that are previously unknown in the better-studied nocturnal European Common Octopus. 

Here we use a comparative approach with a suite of histology, magnetic resonance imagery (MRI), behavioural observations and ecological survey to investigate several understudied octopus groups. New findings from this project shed new light to challenge a longstanding myth that octopuses have a highly conservative brain organisation for their short lifespan and offer non-anthropomorphic insights into how their neural and anatomical adaptations link to advanced cognitive behaviours and sensory ecology. 

This project provides the first detailed description of body patterns expressed during social interactions of the diurnal algae octopus, Abdopus capricornicus. It disentangles the body patterns used for camouflage from those used for communication during intrasexual and intersexual interactions. Aside from their unique social behaviours, intense predatory pressures, particularly from fish and seabirds, likely drive the development of their rich body patterning repertoire for rapid camouflage to avoid threats and intraspecific communication. This mirrors the complexity of their enlarged visual and learning brain lobes with the sulci (increasing surface folding). Remarkably, the flick electroretinogram of the algae octopus showed that their eyes are capable for fast visual tasks (190-200Hz), approximately 3X faster than that of nocturnal octopuses (60-65Hz). The demands of social interactions and other visual tasks in the lit reef likely led to the formation of multiple compartments in the vertical lobe (VL, learning and memory centre) and optic lobe (visual centre) linked to behaviours and ecological niches in ways reminiscent of the vertebrate brain. 

Two nocturnal coastal species, blue-lined octopus (Hapalochlaena fasciata) and red-spot night octopus (Callistoctopus dierythraeus), exhibit simpler body patterning, likely due to their solitary lifestyles and limited social interaction. While both species still rely on camouflage to avoid visual detection, they employ striking aposematic colouration to warn potential predators. In the low-light environments they inhabit, where visual tasks are reduced, these nocturnal octopuses show an enlargement in the chemo-tactile brain region (approximately 6% of the total brain volume) than that of their diurnal siblings (3%). This suggests that chemosensory input plays a more dominant role than vision in guiding their behaviour and foraging. 

Furthermore, unlike the nocturnal common octopus which possesses a 5-gyrus VL such as the blue-lined octopus, the night red-spot octopus possesses two additional subdivisions in the VL as that found in the diurnal reef octopuses. This 7-gyrus VL might be related to their unique burrow-building behaviour, in which they hide in this deep tunnel during the daytime. 

Another major discovery is to unfold sexual dimorphism features in the blue-lined octopus – development of an enlarged venom gland of the petite male. This adaptation is a co-evolutionary arms race between the sexes whereby a cannibalizing large female is counteracted in males through the use of tetrodotoxin (TTX). The use of venom to reduce mating conflicts in mollusks and arthropods is a remarkable example of convergent evolution, whereby a trait that evolved to deter predators and capture prey has been co-opted for reproduction. It also highlights that TTX may have many more roles than previously assumed. 

Four mesopelagic octopus species (telescope-eyed octopus and three species of the glass octopus) have also been imaged using MRI, providing the first-hand evidence of the complexity of their brain organisation and novel eye designs (tubular or non-spherical eyes). This unique dataset provides a timely, new-technology update, uncovering how these rarely explored specimens have evolved their eyesight to the low-light conditions below 500 m depth. 

This project unlocks new ways to analyse, record and model the elements and interactions of neurobiological systems of octopuses, updating knowledge gaps in brain mapping, the functional circuits and the associated behaviours as well as evolutionary history of these advanced and apparently smart molluscs.