Adapted for adaptability-evidence suggests primate brains use reservoir computing

Photo: Christopher Walsh, Harvard Medical School

Primate brains are incredibly adaptive, responding to new situations and stimuli as needed. Think of all of the various skills we learn from computer programming to making pottery to neuroscience. Our brains learn new content and do so relatively efficiently, but how? How are humans and other primates so good at adapting to new information and scenarios?

Enel and colleagues (2016) wanted to better understand how our primate brains adapt to situations and stimuli that evolution could not have directly anticipated. They took advantage of developments from Rigotti and colleagues (2010) in reservoir computing, a branch of recurrent neural networks in which randomly connected neurons form a network of recurrent loops. Recurrent connections are fixed but connections from to output neurons can change. Rigotti and colleagues (2010) propose that recurrent neural networks with multiple, different neuronal responses are significant in the ability to complete complex cognitive tasks.

Enel and colleagues (2016) developed a recurrent neural network model that would perform a specific cognitive task and then compared predictions from the model to data from rhesus monkeys. Of four potential targets on a touch screen, only one would reward the monkeys with fruit juice. The monkeys needed to discover the fruit juice target by trial and error. The target corresponding to fruit juice changed after every trial.

Model Architecture, Figure from Enel and colleagues 2016 paper, Reservoir Computing Properties of Neural Dynamics in Prefrontal Cortex

Results show that the model was able to shift when it did not receive a reward and repeat when it did, a new extension of the functions of reservoir computing. The model was able to perform the task almost perfectly using a circular search and an ordered search and when trained on a schedule that was derived from the performance of one of the monkeys. Enel and colleagues (2016) compared the neural coding behavior of the model with the primate cortex. They found that variance in the presence of reservoir neurons in 1) target choice and 2) phase of the problem (either continue searching to find the reward or repeat because the reward has been discovered) show significant effects for both choice and phase. Choice and phase could not be directly derived from current inputs, but instead needed the history of previous inputs and their responses. This has also been observed for the primate brain (Barone and Joseph, 1989). See the published paper for the full results and more details about their findings.

This new research helps to explain how primates face and then handle a diverse and endless range of situations. It will be interesting to see if the same mechanism for behavioral adaptability is found in non-primate species or if it is unique to primates.

Works cited:

Barone, P., & Joseph, J. P. (1989). Prefrontal cortex and spatial sequencing in macaque monkey. Experimental brain research, 78(3), 447-464.

Enel, P., Procyk, E., Quilodran, R., & Domineer, P., F. (2016) Reservoir Computing Properties of Neural Dynamics in Prefrontal Cortex. PLoS Comput Biol, 12(6): e1004967. DOI: 10.1371/journal.pcbi.1004967 

Rigotti, M., Ben Dayan Rubin, D. D., Wang, X. J., & Fusi, S. (2010). Internal representation of task rules by recurrent dynamics: the importance of the diversity of neural responses. Frontiers in Computational Neuroscience, 4, 24.

Cercopithecus monkeys opportunistically prey on bats

C. mitis, photo Diana Robinson

Two species of Cercopithecus monkeys in Kenya have been observed and documented feeding on bats when the opportunity presents itself. Tapanes and colleagues (2016) photographed and filmed this behavior in Blue monkeys, Cercopithecus mitis, and in one monkey which was a hybrid species of C. mitis and C. ascanius, the Red-tailed monkey. They report on thirteen observations of bat predation attempts over six and a half years at two sites, Gombe in Tanzania and the Kakamega Forest in Kenya). Of these thirteen attempts, eleven were successful. Surveying researchers of blue and red-tailed monkeys at other sites did not identify further instances of bat predation.

Although identifying the bats was challenging, Tapanes and colleagues determined that multiple species of bats were consumed. Researchers observed two instances where an individual grabbed a lone roosting bat and consumed it. In the other observations, the researchers did not witness the individual capturing the bat.

Unsurprisingly, the evidence suggests that bats are a preferred food item for Cercopithecus monkeys. In two of a successful predation event, other monkeys gathered around and observed the monkey feeding on the bat. Three instances were observed where some sort of aggressive display or behavior to either obtain or retain the bat, implying this food item is worth fighting over.

All observed instances of this behavior occurred in either forest edges or human-modified habitat, raising the question as to whether or not this behavior occurs naturally or is a product of habitat destruction and alteration due to human activities. It is possible that anthropogenic changes to the landscape have resulted in blue and red-tailed monkeys altering their feeding patterns and behaviors accordingly, with increased consumption of bats as a potential modification. Thirty-six years of data collection at Kakamega forest show that bat predation coincides with increased use of plantation forests that has occurred due to forest fragmentation and loss. Tapanes and colleagues (2016) also suggest that bat predation could be more widespread, but it is simply easier for researchers to observe this rare behavior within altered habitats. They do not think this reason is likely, stating that observation conditions were similar in both plantation forest and forest that is more natural.

Blue monkey feeding, photo Christoph Strässler

These findings have important implications for the transmission of zoonotic diseases, or diseases that can be transmitted from animals to humans. It has previously been hypothesized that primates contract diseases from bats when they consume fruit with an infected bat's saliva or feces (Dobson, 2005; Alexander et al., 2015; Rodhain, 2015). This latest study forces us to consider the fact that directly handling the bats themselves may be a method for disease transfer. As monkeys can transmit many diseases to humans, it is worth studying this phenomenon more, if possible.

Links of potential interest:
IUCN Redlist page for C. mitis
Primate zoonotic diseases
Which primate is likely the source of the next pandemic?
Ebola, primates, and bushmeat

Works cited:
Alexander, K. A., Sanderson, C. E., Marathe, M., Lewis, B. L., Rivers, C. M., Shaman, J., ... & Eubank, S. (2015). What factors might have led to the emergence of Ebola in West Africa?. PLoS Negl Trop Dis, 9(6), e0003652.
Dobson, A. P. (2005). What links bats to emerging infectious diseases?. Science, 310(5748), 628-629.
Rodhain, F. (2015). Chauves-souris et virus: des relations complexes. Bulletin de la Société de pathologie exotique, 108(4), 272-289.
Tapanes, E., Detwiler, K. M., & Cords, M. (2016). Bat Predation by Cercopithecus Monkeys: Implications for Zoonotic Disease Transmission. EcoHealth, 1-5.

What do geladas and humans have in common? Apparently, vocal patterns.

T. gelada. Photo: Ron Waddington

They live in very large groups called herds, they primarily graze on terrestrial vegetation, and they roam on large open plains. In more than a few ways, geladas (Theropithecus gelada) are similar to cows. Geladas are more vocal than cows though. They have a diverse range of vocalizations for various behaviors and situations, such as contact, showing submission, aggression, and others (Kawai, 1979; Aich et al., 1990).  The diversity and complex communication exhibited by geladas is one of the reasons this is a very interesting primate species to study.

A new study on their vocal sequences shows that this species of Old World Monkey follows patterns that are similar to humans. As far back as the late eighties, Richman (1987) suggested the geladas use melody and rhythm in ways similar to humans. Now, Gustison and colleagues have shown that the longer the sequence of sounds is that a gelada makes, the shorter the sounds within that long sequence. This is the same pattern observed in humans and is called Menzerath's law. The longer our sentences, the shorter the words tend to be in those sentences.

The authors studied fifty-seven male geladas in the wild and recorded and analyzed over 1000 vocal sequences. In addition to discovering that longer sequences are made up of shorter calls, Gustison and colleagues report that long sequences start with short calls and short sequences start with long calls. Thus, the start of the sequence is an indicator of its overall length. Longer sequences also have faster tempos. Gustison and colleagues state this might be to reduce the possibility of one gelada being "talked over" by another. You can understand how this might be a problem in a chatty species that lives on open plains. If you have a lot to say, you better say it quickly.

Geladas grazing. Photo Alastair Rae

Interestingly, there was no negative relationship between the position of a call and its duration (calls later in the sequence were not shorter). Yet, the proportion of grunts where the gelada was exhaling decreased in longer sequences and the proportion of grunts where the individual inhaled increased. The authors believe this pattern is due to the fact that individuals make grunts with both inhalations and exhalations on the same breath as the sequence lengthens. Once geladas have more than 15 calls per sequence, the majority of their calls have both inhale and exhale grunts and the proportion of inhale and exhale grunts hardly varies.  Thus, respiration and energy demands may constrain gelada vocalizations, and be partially the reason for conforming with Menzerath's law.

This is the first time Menzerath's law has been studied in non-humans. Thus, other animals with expansive vocal repertories, such as songbirds, may also exhibit this law. It is hard to draw conclusions about the evolution of communication in non-human primates and our human ancestors without knowing if Menzerath's law holds true for species that are further separated from humans. For now, we know humans are not unique in adhering to Menzerath's law.  It is possible that this pattern existed before meaningful combinations of vocalizations had evolved. Tests in other species will only serve to improve our understanding of sequences, vocal patterns, and the evolution of language and communication in general.



Links of potential interest:
Menzerath's Law
IUCN page on geladas
YouTube video on gelada chatter

Works cited:

Aich, H., Moos-Heilen, R., & Zimmermann, E. (1990). Vocalizations of adult gelada baboons (Theropithecus gelada): acoustic structure and behavioural context. Folia primatologica, 55(3-4), 109-132.
Kawai, M. (1979). Auditory communication and social relations. Ecological and Sociological Studies of Gelada Baboons, 219-241.
Gustison, M., Semple, S., Ferrer-I-Rancho, R, Bergmann, T. (in press). Gelada vocal sequences follow Menzerath’s linguistic law. PNAS. www.pnas.org/cgi/doi/10.1073/pnas.1522072113 
Richman, B. (1987). Rhythm and melody in gelada vocal exchanges. Primates, 28(2), 199-223.