Cephalopod Behavior: From Neural Plasticity to Consciousness

Abstract

It is only in recent decades that subjective experience - or consciousness - has become a legitimate object of scientific inquiry. As such, it represents perhaps the greatest challenge facing neuroscience today. Subsumed within this challenge is the study of subjective experience in non-human animals: a particularly difficult endeavor that becomes even more so, as one crosses the great evolutionary divide between vertebrate and invertebrate phyla. Here, we explore the possibility of consciousness in one group of invertebrates: cephalopod molluscs. We believe such a review is timely, particularly considering cephalopods' impressive learning and memory abilities, rich behavioral repertoire, and the relative complexity of their nervous systems and sensory capabilities. Indeed, in some cephalopods, these abilities are so sophisticated that they are comparable to those of some higher vertebrates. Following the criteria and framework outlined for the identification of hallmarks of consciousness in non-mammalian species, here we propose that cephalopods - particularly the octopus - provide a unique test case among invertebrates for examining the properties and conditions that, at the very least, afford a basal faculty of consciousness. These include, among others: (i) discriminatory and anticipatory behaviors indicating a strong link between perception and memory recall; (ii) the presence of neural substrates representing functional analogs of thalamus and cortex; (iii) the neurophysiological dynamics resembling the functional signatures of conscious states in mammals. We highlight the current lack of evidence as well as potentially informative areas that warrant further investigation to support the view expressed here. Finally, we identify future research directions for the study of consciousness in these tantalizing animals.

Deciphering regeneration through non-model animals: A century of experiments on cephalopod mollusks and an outlook at the future

“…Positioning as “marine Guinea pigs” within the framework of comparative physiology and biochemistry ( Grimpe, 1928 ), the animals were later laboriously consolidated as experimental tools to explore neurone and axon, if not of the brain altogether. The intensive research activity undertaken in the past century allowed for the identification of many cephalopods’ special features, amongst which the complex behavioural and learning capabilities and the intricate and sophisticated nervous system, and the capacity to modulate behavioural responses elicited by stimuli considered potentially painful, stand out ( Nixon and Young, 2003 ; Crook, 2021 ; Ponte et al, 2021 ; Ponte et al, 2022 ). The above-mentioned features supported the inclusion of cephalopods, as the sole invertebrate class, in the Directive 2010/63/EU ( Andrews et al, 2013 ; Smith et al, 2013 ; Fiorito et al, 2015 ; Ponte et al, 2019 ; De Sio et al, 2020 ) regulating the use of animals in scientific research.…”

FELASA Working Group report: Capture and transport of live cephalopods – recommendations for scientific purposes

“…The outcome of this analysis is not provided herein but is presented in detail in the ancillary work. 2 The analysis of the available information highlighted important considerations:…”

“…Over the last decades, discoveries about cephalopod biological, evolutionary, morphological, genomic and physiological innovations and adaptations, as well as their neural and cognitive characteristics, have promoted a renewed interest for these animals, favouring the increase in the number of studies and species utilised for scientific purposes. [1][2][3][4][5][6] At the same time, the relevance of their welfare status 7,8 and its consequences on the scientific outcome have increased in both the commercial and the scientific fields.…”

Evolution of neuroglia

“…These are interlaminar, polarized, and varicose projection astrocytes. Interlaminar astrocytes (Figure 5) have a small cell body (∼10 μm) localized in layer I of the cortex and several short and one or two very long (up to 1 mm) processes, which penetrate through the cortex and end in layers II to IV 55,56 . The soma of polarized astrocytes is localized in the deep cortical layers close to the white matter.…”