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fNIRS in animal research

By Rens Burghardt

As our community has grown considerably throughout the years, it’s worth taking a step back to explore the many different, and perhaps surprising, ways that research is conducted in our field. Here, we briefly explore the different uses of fNIRS in animal research and opportunities for using fNIRS in animal monitoring in particular.

fNIRS FOR VETERINARIANS?

While Elon Musk’s Neuralink received much positive media coverage since its inception, news broke this February that the company is under investigation for alleged safety violations following earlier reports on alleged animal welfare violations last December. A stark contrast from the prevailing excitement surrounding Neuralink’s first live stream update in 2020. This public event included demonstrations of a pig walking on a treadmill while intracranial neural recordings measured and predicted planned joint movements. Although the engineering element of the overall presentation appeared to have been received positively by experts in the field, the science aspect wasn’t deemed a step change (e.g., see here and here). The event did generate much interest from the general public in brain-computer interfaces (BCIs).

Even though Neuralink aims to develop BCIs that support individuals with paralysis, it is not hard to envision how BCIs could aid animal welfare (e.g., see Neethirajan, 2022). Unsurprisingly, some companies have introduced wearables that monitor specific physiological functions like blood pressure and heart health for veterinarians and ‘smart farms’. BCI applications are not at this stage, but there is potential to use BCIs to monitor animal behaviors such as feeding, sleeping, and social interactions. These measures might help to inform abnormality detection, medical treatments, and environmental enrichment. EEG and intracranial EEG have shown some opportunities to serve these goals. But could we make a compelling case for fNIRS?

fNIRS IN ANIMAL RESEARCH

Intracranial EEG is often deemed the go-to solution for most BCI applications. It’s a technique that generally achieves superior sensitivity and specificity compared to fNIRS. Yet fNIRS-based hemodynamic decoding might have unexpected advantages over intra- and extracranial neural decoding. fNIRS is safer, non-invasive, and arguably applicable at lower costs than brain implants. Implantation procedures and subsequent medical monitoring render brain implants impractical for specific situations and unethical when viable alternatives exist. After all, BCIs can adopt fNIRS as a wearable; brain implants cannot be a wearable. Action potentials propagate much faster than hemodynamic responses, but timing is hardly a consideration when monitoring slow behaviors more akin to mental states such as pain experience, stress, sleeping, and social interactions. Extracranial EEG could provide matching mental state measures, but the equipment might arguably be less suitable for long-term monitoring. In sum, there might be contexts in which fNIRS could play a key role in animal BCI applications. But what steps have been taken so far? What role has animal research played in the fNIRS field so far?

Research in fNIRS wearables for animal monitoring is relatively new (e.g., see Kim et al. 2017; Ruesch et al., 2022b), but fNIRS research with animal subjects has obvious precedent. See Ferrari & Quaresima (2012) for a brief coverage of animal models within the historical development of fNIRS. The literature review reported in Kim et al. (2017) provides an overview of more recent animal studies until 2017. These studies mainly focused on testing animal models and validating fNIRS (e.g., vis-à-vis other invasive and non-invasive neuroimaging modalities). The experiments primarily tested macaque monkeys, rats, and mice. Rodents typically received relatively tiny optodes on either the brain or skull. While this procedure works within the aims of these studies, it does not make a proof of concept for fNIRS wearables straightforward. An informal and cursory search for publications after 2017 did not find reviews discussing fNIRS research aimed at animal model testing or validating fNIRS. Some reports on individual experimental studies were added to the literature after 2017. 

Another research strand that appears to have benefited from fNIRS in animal subjects aims to investigate animal cognition. These studies are typically conducted in controlled laboratory settings and have thus far used cognitive tasks to test especially non-human primates and sheep. A good illustration is the study reported in Debracque et al. (2022). Here, the authors observed hemodynamic responses in three captive female baboons and found differences across stimulus conditions. These conditions consisted of audio recordings of combative calls made by either baboons or another species: chimpanzees. Characteristic of animal cognition studies, results were compared with human studies and discussed in light of evolutionary theory. An informal and cursory search did not find many fNIRS studies measuring animal cognition for the sake of understanding animal cognition itself. Most studies use cognitive measures for other aims: animal model testing or observing free-ranging animals using fNIRS wearables.

The third and perhaps final identifiable research strand centers around observing free-ranging animals. These studies typically aim to demonstrate a proof of concept for an fNIRS wearable that monitors pet animals or animals in either wildlife or managed facilities, like farms. A recent review in Ruesch et al. (2022b) demonstrated the feasibility of monitoring marine mammals, i.e., seals, a dolphin, and, well, human freedivers. An informal and cursory literature search did not find research aimed at wildlife tracking. Perhaps the closest step taken to that effect was a study with four previously caught juvenile seals (McKnight et al., 2019). Besides marine mammals, previous publications have reported on studies using fNIRS wearables for dogs, sheep, and goats (see Kim et al., 2017). Amusingly, the system in these studies was generally termed wireless fNIRS in the literature but termed wearable fNIRS in more recent reporting. While studies have demonstrated the feasibility of fNIRS measurements in free-ranging animals since the 2010s, no application appears currently in use outside research. An important step toward such applications could be research demonstrating the feasibility and added value of decoding fNIRS measures to specific problems and contexts.

An informal and cursory search found only one fNIRS study that decoded animal hemodynamic responses (Im et al., 2022). It’s unlikely that decoding animal hemodynamic responses is infeasible given the ongoing demonstrations of BCI applications in human participants.

CHALLENGES AND OPPORTUNITIES

A recent conference paper by Ruesch et al. (2022a) on light propagation in dolphin blubber might hit the nail on the head: nearly every wearable application has unique challenges. fNIRS is limited to species and age groups with adequate brain size and physiologies that allow for fNIRS’s depth penetration. Also, not all animals are keen on carrying a wearable. Light anesthetization can help but is not optimal in most contexts, let alone for (long-term) animal monitoring. The wearer’s bias is reducible by repeated exposure, but some species might still have the limbs or help from nimble friends to confiscate the device and put it to other uses… And perhaps most importantly, we know far less about the neural underpinnings of animal behavior and mental states in most animal species than we do for humans, never mind about hemodynamic responses.

Yet the wide range of opportunities in animal monitoring using fNIRS wearables is notable. While no firm seems to have published market research on fNIRS-based BCIs for pets and pet owners… It might not be a far-flung idea. An fNIRS wearable might also be applicable for livestock monitoring for veterinarians and tomorrow’s “smart farms”. For example, CCTV is the current gold standard in monitoring pregnant farm animals. While machine learning-based CCTV could carry some of the burden in monitoring livestock, fNIRS and other wearables could take it further by directly measuring physiological changes. An fNIRS wearable might also be worth considering in monitoring and researching wildlife. Ecological validity is maintained because animals are not interrupted during monitoring — a boon to tracking endangered species and reintroducing species to their natural habitat. Of course, depending on the questions asked, other wearables could also be of use. Even a camera at anterior presentation can provide surprising data… 

Although it is early days for fNIRS wearables in animal monitoring, the literature shows that fNIRS can play a unique role in a field opening up to BCIs and wearables.

As our community has grown considerably throughout the years, it’s worth taking a step back and explore the many different and, perhaps, surprising research avenues in our field. This time, we briefly explored the different uses of fNIRS in animal research and opportunities in using fNIRS for animal monitoring in particular. Do you have any questions, tips, or commentaries on this feature? Are there studies that should be in this feature? Please let us know. You can email the Communications Committee (commcomm@fnirs.org) or the author (reburghardt@surgery.cuhk.edu.hk). Your comments are much appreciated.

REFERENCES

  • Debracque, C., Gruber, T., Lacoste, R., Meguerditchian, A., & Grandjean, D. (2022). Cerebral activity in female baboons (Papio anubis) during the perception of conspecific and heterospecific agonistic vocalizations: A functional near infrared spectroscopy study. Affective Science, 3, 783-791. https://doi.org/10.1007/s42761-022-00164-z
  • Ferrari, M., & Quaresima, V. (2012). A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application. Neuroimage, 63, 921–935. https://doi.org/10.1016/j.neuroimage.2012.03.049
  • Franceschini, M. A., Nissilä, I., Wu, W., Diamond, S. G., Bonmassar, G., & Boas, D. A. (2008). Coupling between somatosensory evoked potentials and hemodynamic response in the rat. NeuroImage, 41, 189-203. https://doi.org/10.1016/j.neuroimage.2008.02.061
  • Im, C, Shin, J., Lee, W. R., & Kim, J. M. (2022). Machine learning-based feature combination analysis for odor-dependent hemodynamic responses of rat olfactory bulb. Biosensors and Bioelectronics, 197, 113782. https://doi.org/10.1016/j.bios.2021.113782
  • Kim, H., Seo, K., Jeon, H., Lee, U., & Lee, H. (2017). Application of functional near-infrared spectroscopy to the study of brain function in humans and animal models. Molecules and Cells, 40, 523-532. https://doi.org/10.14348/molcells.2017.0153
  • McKnight, J. C., Bennett, K. A., Bronkhorst, M., Russell, D. J. F., Balfour, S., Milne, R., Bivins, M., Moss, S. E. W., Colier, W., Hall, A. J., & Thompson, D. (2019). Shining new light on mammalian diving physiology using wearable near-infrared spectroscopy. PLoS Biology, 17, e3000306. https://doi.org/10.1371/journal.pbio.3000306
  • Neethirajan, S. (2022). Affective state recognition in livestock—Artificial intelligence approaches. Animals, 12, 759. https://doi.org/10.3390/ani12060759
  • Ruesch, A., Acharya, D., Bulger, E., McKnight, J. C., Fahlman, A., Shinn-Cunningham, B. G., & Kainerstorfer, J. M. (2022a). Light propagation through dolphin blubber: Towards marine mammal NIRS [Poster Presentation]. Optical Tomography and Spectroscopy 2022, Fort Lauderdale, Florida, United States. https://doi.org/10.1364/TRANSLATIONAL.2022.JM3A.15
  • Ruesch, A., McKnight, J. C., Fahlman, A., Shinn-Cunningham, B. G., & Kainerstorfer, J. M. (2022b). Near-infrared spectroscopy as a tool for marine mammal research and care. Frontiers in Physiology, 12, 816701. https://doi.org/10.3389/fphys.2021.816701