4.2 Review

Cephalopod Behavior: From Neural Plasticity to Consciousness

Journal

FRONTIERS IN SYSTEMS NEUROSCIENCE
Volume 15, Issue -, Pages -

Publisher

FRONTIERS MEDIA SA
DOI: 10.3389/fnsys.2021.787139

Keywords

cephalopods; behavioral plasticity; cognition; consciousness; neural plasticity

Categories

Funding

  1. Stazione Zoologica Anton Dohrn
  2. Association for Cephalopod Research CephRes

Ask authors/readers for more resources

In recent decades, the study of subjective experience or consciousness has become a legitimate object of scientific inquiry, posing one of the greatest challenges for neuroscience. This paper explores the possibility of consciousness in cephalopod molluscs, particularly the octopus, based on their impressive learning and memory abilities, neural substrates, and neurophysiological dynamics resembling conscious states in mammals.
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.

Authors

I am an author on this paper
Click your name to claim this paper and add it to your profile.

Reviews

Primary Rating

4.2
Not enough ratings

Secondary Ratings

Novelty
-
Significance
-
Scientific rigor
-
Rate this paper

Recommended

Review Physiology

Can Cephalopods Vomit? Hypothesis Based on a Review of Circumstantial Evidence and Preliminary Experimental Observations

Antonio Sykes, Eduardo Almansa, Giovanna Ponte, Gavan M. Cooke, Paul L. R. Andrews

FRONTIERS IN PHYSIOLOGY (2020)

Article Anatomy & Morphology

Cerebrotypes in Cephalopods: Brain Diversity and Its Correlation With Species Habits, Life History, and Physiological Adaptations

Giovanna Ponte, Morag Taite, Luciana Borrelli, Andrea Tarallo, A. Louise Allcock, Graziano Fiorito

Summary: This study analyzes existing quantitative data on cephalopod brains and identifies ten clusters grouping 52 species. Attempting a phylogenetic PCA reveals limited impact due to the small number of species considered. Preliminary findings suggest that brains in cephalopods evolved based on factors such as phylogeny, possible development, and lifestyle adaptations.

FRONTIERS IN NEUROANATOMY (2021)

Article Cell Biology

Imaging Arm Regeneration: Label-Free Multiphoton Microscopy to Dissect the Process in Octopus vulgaris

Pamela Imperadore, Roberta Galli, Martin J. Winterhalder, Andreas Zumbusch, Ortrud Uckermann

Summary: This study applied label-free imaging technique to investigate the injured arm of Octopus vulgaris, revealing the tissue architecture and elements of the arm, as well as providing morpho-chemical information about the regenerative phases. This method shows potential for regenerative studies in cephalopods and other non-model species.

FRONTIERS IN CELL AND DEVELOPMENTAL BIOLOGY (2022)

Article Biology

Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain

Giuseppe Petrosino, Giovanna Ponte, Massimiliano Volpe, Ilaria Zarrella, Federico Ansaloni, Concetta Langella, Giulia Di Cristina, Sara Finaurini, Monia T. Russo, Swaraj Basu, Francesco Musacchia, Filomena Ristoratore, Dinko Pavlinic, Vladimir Benes, Maria I. Ferrante, Caroline Albertin, Oleg Simakov, Stefano Gustincich, Graziano Fiorito, Remo Sanges

Summary: This study identifies transposable elements with retrotranspositional competence in Octopus vulgaris and Octopus bimaculoides, and shows evidence that they are transcribed and may determine germline and somatic polymorphisms, especially in the brain. The study also reports the transcription of thousands of putative lncRNAs and the inclusion of TE fragments in the transcriptomes of both octopus species, highlighting the crucial activity of TEs in the evolution of octopus genomes.

BMC BIOLOGY (2022)

Review Veterinary Sciences

General and species-specific recommendations for minimal requirements for the use of cephalopods in scientific research

Giovanna Ponte, Katina Roumbedakis, Viola Galligioni, Ludovic Dickel, Cecile Bellanger, Joao Pereira, Erica Ag Vidal, Panos Grigoriou, Enrico Alleva, Daniela Santucci, Claudia Gili, Giovanni Botta, Pamela Imperadore, Andrea Tarallo, Lars Juergens, Emily Northrup, David Anderson, Arianna Arico, Marianna De Luca, Eleonora Maria Pieroni, Graziano Fiorito

Summary: In this article, species-specific recommendations for the housing, care, and management of cephalopod mollusks employed for research purposes are listed, with the aim of standardizing the minimum requirements for their establishments, care, and accommodation in compliance with Directive 2010/63/EU. The prioritization of maximizing their psychophysical welfare is emphasized. The general recommendations on water surface area, water depth, and tank shape provided here are based on an analysis of available literature and a consensus reached among researchers working with the most commonly used cephalopod species in Europe, under the COST Action FA1301. Information on water supply and quality, environmental conditions, stocking density, feeding, and handling is also included. Through this work, the authors hope to promote evidence-based approaches to cephalopod laboratory maintenance, facilitating standardization and replicability of research outcomes across laboratories, while also maximizing the welfare of these animals.

LABORATORY ANIMALS (2023)

Review Physiology

Methodological considerations in studying digestive system physiology in octopus: limitations, lacunae and lessons learnt

Paul L. R. Andrews, Giovanna Ponte, Carlos Rosas

Summary: Current understanding of cephalopod digestive tract physiology is mainly based on older literature and data from multiple species. The anatomical differences between cephalopod species caution against extrapolating data on digestive system physiology. An overview of anatomy and histology techniques is provided, followed by a review of current knowledge on major digestive tract functions and the techniques used to study them. Knowledge gaps are identified, calling for more systematic research in this field.

FRONTIERS IN PHYSIOLOGY (2022)

Article Multidisciplinary Sciences

Cell type diversity in a developing octopus brain

Ruth Styfhals, Grygoriy Zolotarov, Gert Hulselmans, Katina I. Spanier, Suresh Poovathingal, Ali M. Elagoz, Seppe De Winter, Astrid Deryckere, Nikolaus Rajewsky, Giovanna Ponte, Graziano Fiorito, Stein Aerts, Eve Seuntjens

Summary: This study analyzed the cell types in the octopus brain and constructed a cell type atlas. The research found that the octopus brain has diverse cell types, which share common gene features with cell types in other species. Additionally, transcriptionally related cell types were found in different brain regions.

NATURE COMMUNICATIONS (2022)

Review Cell Biology

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

Fabio De Sio, Pamela Imperadore

Summary: The establishment of marine stations in the late 19th century has enabled biologists to study many marine organisms, and cephalopod mollusks have drawn attention due to their adaptability to captivity and unique features including sophisticated behavior and complex nervous system. However, the study of tissue regeneration in cephalopods has been limited despite its centuries-old knowledge. This article reviews previous studies, discusses the peripherality of cephalopods in regeneration research, and explores the growing relevance of cephalopods as models for regeneration in contemporary biology and medicine.

FRONTIERS IN CELL AND DEVELOPMENTAL BIOLOGY (2023)

Article Neurosciences

Transcriptome-wide selection and validation of a solid set of reference genes for gene expression studies in the cephalopod mollusk Octopus vulgaris

Pamela Imperadore, Stefano Cagnin, Vittoria Allegretti, Caterina Millino, Francesca Raffini, Graziano Fiorito, Giovanna Ponte

Summary: The study selected 77 candidate reference genes, evaluated their expression stabilities in different tissues, and identified Ov-RNF7, Ov-RIOK2, Ov-EIF2A, and Ov-CUL1 as stable reference genes for various tissues. The expression profiles of nine target genes in different areas of the octopus nervous system were validated using these reference genes.

FRONTIERS IN MOLECULAR NEUROSCIENCE (2023)

Editorial Material Physiology

Editorial: Methods and applications in invertebrate physiology

Natraj Krishnan, Tetsuya Tanaka, Graziano Fiorito, Fernando Ariel Genta, Pamela Imperadore

FRONTIERS IN PHYSIOLOGY (2023)

Article Veterinary Sciences

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

Antonio Sykes, Viola Galligioni, Juan Estefanell, Stuart Hetherington, Marco Brocca, Joao Correia, Andre Ferreira, Eleonora M. Pieroni, Graziano Fiorito

Summary: This article discusses research on cephalopod molluscs and the challenges of captive breeding. The need for specific recommendations on the capture and transport of these animals is highlighted. The authors provide suggestions for standardized assessment methods and a training program.

LABORATORY ANIMALS (2023)

No Data Available