NSF grant awarded to the lab to study neural mechanism of injury-induced behavior

PI Robyn Crook awarded NSF CAREER grant

Our lab’s work has been funded by the NSF for the next five years, to continue our work on elucidating neural mechanisms of plasticity that underlie injury-induced behaviors in cephalopods. This grant includes funding for studies looking at fitness effects of injury-induced behavior in contexts that have not previously been studied, such as in mating and reproductive success. Other experiments are focused on mapping and characterizing nociceptive sensory neurons in the peripheral ganglia and central brains of cephalopods, and continued work supporting welfare-based refinements to experimental procedures using cephalopods. This grant mechanism (NSF CAREER) also includes support for educational work and outreach that our lab already does regularly, so this will allow us to grow these efforts to support neuroscience training for students in the Department of Biology, and continue our work engaging pre-K children in STEM.

Crook Lab research featured in Scientific American Magazine

Scientific American Magazine 4.23.21

Our recent paper on pain experience in octopus features in a new article out today in Scientific Amercian Magazine. The article describes a scene in the recent documentary “My Octopus Teacher” where the octopus survives a predation attempt but loses an arm in the process; this type of injury is exceptionally common in wild cephalopods. Our lab’s research on physiological responses to injury in cephalopods supports the idea that cephalopods have a similar experience of pain as mammals after tissue injury, and that similar welfare protections for cephalopods in fisheries and research are warranted. Read the article here.

Megan's paper on giant Pacific octopus welfare in the news!

A Giant Pacific Octopus interacts with a caretaker

While Meghan Holst was completing her MS degree in our lab she was also working on a long-running project developing an objective welfare assessment tool for giant Pacific octopuses held in public aquaria, with the goal of improving decision-making around end-of-life care and euthanasia. Her work was published late last year in the Journal of Applied Animal Welfare Science, and recently has been featured on the Oregon State University news page (link to the news story and interview with the authors is here). Meghan graduated from the MS program here in 2020 and is currently working toward her PhD at UC Davis, and also continues her work at the Aquarium of the Bay in San Francisco.

It’s great to see the continued success of the Crook Lab’s outstanding student alumni!

New publication: Pain experience in octopus

Octopus bocki explores in an Condition Place Preference chamber, where visual cues link an experience with a particular context. ©CrookLab

The newest work from our lab has just been published in iScience. In this study, we show that octopuses demonstrate behaviors that strongly indicate that they are able to experience the affective, or emotional, component of pain. These finds are a significant advance for cephalopod welfare - it is the first clear demonstration of this ability in cephalopods even though there has been ongoing conjecture about such abilities for a many years. This study also provides a framework through which welfare-promoting interventions, like analgesics, can be assessed objectively. More about our work on pain and welfare can be found here. The paper is available open access from iScience, and a news report on the work is available from Academic Times.

Congratulations Meghan!

Meghan Holst defends her thesis by Zoom

Congratulations to Crook Lab MS student Meghan Holst, who successfully defended her thesis titled “Behavioral and neural indicators of welfare in senescent giant Pacific octopus, Enteroctopus dofleini”. Meghan’s project involved a multi-site behavioral study of GPOs in zoos and aquariums across the USA, along with analysis of histological samples from euthanized GPOs. Her data indicate significant new concerns for animal welfare at the early stages of senescence, and raise many new questions about how and when the nervous system declines to the point that these animals are no longer experiencing acceptable quality of life in captive settings.

Her wonderfully successful defense was a great way to cap off a year that has been exceptionally challenging both for research labs like ours and for public zoos and aquariums across the country where her research subjects were housed. Meghan has already started her PhD work at UC Davis and continues to work at Aquarium of the Bay, so we look forward to many more great things from her as she continues her research career.

Do zombies feel pain? An interview with Dr. Zed

Do zombies feel pain? While it’s not a question the lab has previously considered, it’s a hot topic in the world of zombie enthusiasts! What is it about 'zombification’ that makes zombies seemingly insensible to pain, and what would the ethics of experimenting on zombies be? Dr. Crook spoke to Dr. Zed (aka Joe Alcock, an emergency medicine physician at Arizona State University), about pain research, how infectious agents can inactivate pain to gain an advantage over the host, and how an evolutionary perspective on pain can shed new light on pain treatments for humans (and zombies, presumably). A fun outreach event to a very different audience! A replay of the segment on Channel Zed can be found here on YouTube.

New pre-print posted; pain in octopus

An octopus explores the Conditioned Place Preference box. ©CrookLab

Whether cephalopods (and other invertebrate animals) can experience the emotional, affective component of pain (i.e., to know that a noxious sensation is unpleasant or distressing, rather than simply responding via unconscious, behavioral reflex), has always been an unresolved question. The newest work from our lab uses a widely validated assay for studying the affective component of pain in laboratory rodents, to show that octopuses behave the same way. The most parsimonious explanation for the behavior of the octopuses in this experiment is that they are capable of the negative affective state that characterizes pain experience in mammals. This is the first conclusive evidence for this capacity in any invertebrate.

Knowing the answer to this question is more than just a scientific curiosity; it is essential to advancing moves to treat cephalopods more humanely in whichever context they encounter humans - in research labs, but also in zoos, aquariums and in fisheries.

We recognize that research work on pain in animals like cephalopods, with their highly complex brains, is controversial. However, the lack of clarity on the question of whether invertebrate animals can suffer as a result of noxious sensory input continues to hamper efforts to improve their welfare. Our goal with this study was to move the question of invertebrate pain beyond reasonable doubt, so that efforts to better regulate their humane use can proceed with a strong evidentiary foundation that until now, has been lacking.

Evidence for vertebrate-like pain experience in invertebrates has been inconsistent and focused mostly on crustaceans and insects. Some studies supported the hypothesis that the emotional component of pain was present in invertebrates and some did not; there have been very few studies that took validated assays for measuring pain in vertebrate animals and applied them to invertebrates, leaving room for the interpretation that the experimental evidence was insufficient proof of an equivalent emotional state underlying equivalent behavior. In this paper we show that not only can vertebrate specific protocols for testing pain’s presence and absence be adapted to cephalopods, they can reveal the same evidence for internal state.

Octopuses in Pre-K education outreach

CrookLab octopuses visit a local daycare center

Little hands and gentle touches!

Lots of fun today as some of the lab’s retired octopuses visited a local daycare center, to provide an early childhood education experience for the children and staff. Children were able to observe the octopuses up close while the octopuses moved about in shallow tubs that provided shelters and hiding spaces. Whenever we do outreach activities like this we work hard to ensure that the animals’ welfare needs are balanced against the goals of an up-close-and-personal interaction for the children. This visit was a great success!

New Publication: Environmental estrogen affects nociception and behavior in Euprymna scolopes

3do hatchling of Euprymna scolopes exposed to ethynl estradiol. ©CrookLab

Congratulations to Crook Lab MS graduate Stephanie Bazarini, who published her work titled “Environmental estrogen exposure disrupts sensory processing and nociceptive plasticity in the cephalopod, Euprymna scolopes”, this week in the Journal of Experimental Biology. This paper is based on Stephanie’s Masters thesis, in which she combined her interests in the role of estrogens in pain plasticity, and in comparative neurobiology of pain.

Her work demonstrates that both constant, low exposure , and brief, high-level exposure to synthetic estrogen in seawater can have detrimental effects on injury-induced neural and behavioral plasticity. Cephalopods like Euprymna scolopes are exceptionally vulnerable to predation, to injury and to coastal pollutants, and her study shows that these factors combine in ways that are likely to disrupt adaptive behaviors. Her work also suggests that estrogen’s role in modulating pain neural circuits extends beyond vertebrates, a highly novel and important finding for comparative and evolutionary neuroscience.

Congratulations Stephanie!!

Do oysters feel pain? PI Robyn Crook discusses on French radio

Oysters are unlikely to feel pain

The French-language Science program “Science et Vie” fielded a listener question that asked “Do oysters feel pain?” Dr. Crook gave her opinion on this question by discussing the nervous system of oysters, the difference between nociceptive reflexes and the emotional response of pain, and ultimately the presenter reassured the listener that pain experience in oysters is extremely unlikely. Text and audio of the segment (in French) can be found here

Congratulations Meghan!

Meghan Holst

Crook Lab MS student Meghan Holst has been admitted to the PhD program at UC Davis, where she will work in the Durand Lab to continue her ongoing studies of seven-gill shark populations in the SF Bay. Meghan will continue her position at the Aquarium of the Bay during her PhD studies, and hopes to combine her public outreach and conservation work there with her new focus on high-level marine ecosystem research. Congratulations Meghan!!!

Alumni Update - Ryan Howard catches a giant squid!

Ryan Howard directs a dissection of a giant squid, Architeuthis dux, on board the RV Tangaroa

Crook Lab alumnus Ryan Howard (MS Marine Biology, 2019) is currently a PhD candidate at the Aukland University of Technology, where he is studying adaptations in the visual system of deep-sea squid. Ryan has recently returned from a research expedition to Chatham Rise (off New Zealand’s coast), where the vessel caught a giant squid, Architeuthis dux, for his research. Ryan sent us some photos of the dissection process to obtain samples for multiple research projects, and the catch made headlines across New Zealand.

AUT News NZ Herald Stuff.co.nz NZ news1

It’s so exciting to see the amazing work our former students are doing as they move on with their careers!

Alumni Update - Congratulations Rob!

Rob Veline

Crook Lab alumnus Robert Veline (BS Physiology, 2016) has been admitted to the PhD program in Neuroscience at the City University of New York. Rob worked in the Crook Lab as an undergraduate research fellow, where he led a study of learning and memory in Euprymna scolopes. A paper describing operant conditioning in Euprymna was published in the Biological Bulletin in 2017. Since graduating from SFSU, Rob has been working in the auditory neuroscience lab of Professor Michael Brainerd at UCSF. We wish him well in his studies in New York City!

Dr. Crook on KCBS radio on the ethics of octopus farming

Dr. Robyn Crook on KCBS radio

This morning Dr. Robyn Crook was interviewed on KCBS radio during a segment on the emerging controversy around efforts to develop farming methods for octopus. There is considerable interest in developing new technologies for supplying reliable sources of food to the world’s growing population, and octopuses are appealing because they grow quickly and are high in protein. However, several recent articles have focused on the ethical implications of creating an industry exploiting intelligent, potentially conscious species such as octopus. In addition to discussing ethical concerns and methods of humane killing, as well as the ecological implications of in-shore intensive aquaculture of cephalopods.

Congratulations Ryan!!

Ryan Howard profile pic

Congratulations to Ryan Howard, who graduated from the Crook Lab in May 2019, on his admission to the PhD program in Biology at the Aukland University of Technology in New Zealand!!

Ryan will be working with well-known cephalopod biologist, Dr. Kat Bolstad, who runs the ALCES lab at AUT. He will be conducting research on the retinal anatomy of deep-sea oegopsid squid. His surveys of retinal structure across a range of species from diverse habitats will provide novel comparative information on the visual capabilities of cephalopods inhabiting disparate light conditions. The survey will include (1) species that remain in coastal and/or shallow (brightly lit) waters throughout their lives, whose eyes should therefore be able to accommodate the high light

intensities of day-time as well as night-time conditions; (2) species that spend their entire lives at great depth and are therefore presumably never exposed to daylight; (3) species that are able to migrate vertically between photic and aphotic waters over a short period of time, e.g., on a daily basis; and (4) species that inhabit shallow waters during early life stages and descend into the deep sea with maturity.

We wish Ryan all the best with his new adventures in New Zealand!!

New Publication: Early-Life Injury in Squid

Neuroscience of injury in Euprymna scolopes on Phil Trans cover

Congratulations to MS graduate Ryan Howard, and BS (Physiology) Graduates Lauren Lopes, Christina Lardie and Paul Perez, for publishing their work titled “Early life injury produces lifelong neural hyperexcitability, cognitive deficit and altered defensive behavior in the squid, Euprymna scolopes” in Philosophical Transactions of the Royal Society B. It is part of a special issue on the evolution of mechanisms relation to pain. This paper has a long story in our lab; Lauren and Christina first worked on this project in 2016, when we set out to look at the time course of behavioral changes after injury in juvenile squid. When we found nothing much of note in the 2-3 weeks after injury, we let the squid grow to adults for breeding. We also used some of them for an

electrophysiological study on an unrelated question once they were adults, and Lauren and Paul discovered the life-long sensitization of primary afferents in the squid that had received injury as small juveniles. But, after an unexpected power failure led to the loss of our breeding colony of Euprymna in 2017, the project was put on hold for almost 2 years. Ryan picked it up again in early 2019 and conducted the behavioral assays on a new cohort of adults, showing cognitive effects, and finally we were able to make this wonderful paper come together. Well done to all authors for their perseverance and hard work!!

Congratulations Hanna!!

Hanna Butler Struben

Crook Lab Masters student, Hanna Butler-Struben, was accepted into the PhD program in Animal Behavior at UC Davis. Hanna graduated from SFSU with her Masters degree in 2018. She will be working in the field of applied animal welfare. Using her knowledge in pain physiology, she will study how injury can affect behavior and cognition in dairy cattle. Having an applied focus to her project, the ultimate goal is to create better welfare practices that can be used by the dairy industry. Congratulations Hanna!!

Crook Lab research on German Public Radio

The Crook Lab’s research on cephalopod brains, pain and the evolution of complex cognitive states was profiled on German Public Radio, in an article titled “Aliens in the Ocean” about new advancements in understanding the evolution of complex brains using cephalopod mollusks. (article and audio in German)

Can Plants Learn? SFSU biology faculty mentioned in Discover Magazine

“Plant cognition” is a hot topic. Whether plants can learn about and remember their prior experiences is the subject of several recent research studies proposing that classical conditioning occurs in pea and mimosa plants. Professors Andy Zink and Robyn Crook were mentioned in a recent article in Discover Magazine outlining the controversy and problems replicating these astounding results.

Congratulations Stephanie!!

Stephanie Bazarini celebrating with champagne!

Congratulations to Stephanie Bazarini, who successfully defended her thesis titled “Effects of ethinyl estradiol on injury-induced plasticity in Euprymna scolopes” on May 22nd. Stephanie’s work showed that exposure to both low and high doses of this environmental pollutant interferes with neural plasticity and alters behavioral maturation in squid; the first time that an effect on sensory physiology has been reported in cephalopods exposed to environmental estrogens. Stephanie will spend the summer collecting some additional data on neuroanatomy in her subjects, and will be applying to PhD programs in the Fall. Great work Stephanie!