Systems underlying human and nonhumanprimate communication:
One, two, or infinite
Frontiers Pscyhology, 03 Septmeber 2019
Shigeru Miyagawa and Esther ClarkeMITU. Durham/MITOctober 2019

The source of infinity• What is the source of infinity observable in human language?
• Can we learn anything from looking at the communication
system of primates?

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Evolution of the neural language network
Fitch & Hauser (2004) compared artificial grammar learning between human andnonhuman primates using FSG and PSG grammar types. Testing cotton-top tamarins
and human adults in a behavioral grammar learning study, they found that humans
were able to learn both grammar types easily, whereas the monkeys were only able tolearn the FSG.

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Neuroanatomical difference
A functional magnetic resonance imaging (fMRI) study in humanadults using the same type of grammars was conducted (FNG vsPSG). The data revealed different activation patterns for theprocessing of (AB)n sequences and AnBn sequences (Friederici etal., 2006). Sequences of the PSG activated the posterior portionof Broca’s area (Brodmann area [BA 44]) and the frontaloperculum, whereas sequences of the FSG only activated thefrontal operculum. Because the frontal operculum is aphylogenetically older brain region (Amunts & Zilles, 2012;Sanides, 1962), the fMRI results in humans may reflect anevolutionary trait.
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Brodmann’s Area 44
Brodmann area 44, or BA44, is part of the frontal cortex in thehuman brain.

Together with left-hemisphere BA 45, the left hemisphere[1] BA
44 comprises Broca's area, a region involved in semantic tasks.
Some data suggest that BA44 is more involved in motor aspect ofspeech. Some recent findings also suggest the implication of thisregion in music perception.
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Frontal operculum
The frontal operculum is a phylogenetically older part of thebrain compared to the Broca’s area (Sanides 2019), and one of its
functions is apparently to create sequences of (AB) combinations(Friederici et al. 2006).

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BA 44 and hierarchical structure
The specific function of BA 44 and the frontal operculum for thecomputation Merge has been investigated in a series of fMRIstudies (Zaccarella & Friederici, 2015a, b). It was found that
although the frontal operculum/anterior insula supports thebinding of two elements independent of any phrase structure,
BA 44 is recruited only if a hierarchical phrase structure is built.
This indicates that BA 44 is the region in the inferior frontal gyrusthat particularly subserves syntactic hierarchy building.

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αβMiyagawa July 20199

Human and non-human primate brain circuitry
Human and nonhuman primates differ in their abilities to process complex sequences. So far, apart from humans, there is noevidence that other species can process and learn hierarchicallystructured sequences similar to those of natural languages(Beckers, Bolhuis, Okanoya, & Berwick, 2012; Poletiek, Fitz, &Bocanegra, 2016; Yang, 2013). A possible explanation for thisbehavioral difference may lie in the neural differences between

humans and nonhumans with respect to language-related brainstructures.
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Alarm calls of monkeys
It is typically believed that alarm calls are composed ofacoustically distinct, isolated utterances of alarm, such as“leopard,” “eagle,” and “snake” (Blumstein et al. 1999). They do
not combine, for example, “leopard” and “eagle” to create anovel utterance.

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Conveying meaning in the animal world

Vervet monkeys of Kenya(Seyfarth, Cheney, Marler 1980 Science)eagle 鷲snake へびleopardレパード

bees
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General issues regarding alarm calls
Based on:“Survivor signals: The biology and psychology of animal alarm calling” 2009.
Klaus Zuberbüler

Cacophy of alarm calls for leopard
Continuous sound; difficult to divide

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Evidence for mental representation with alarm calls:
Diana monkeys
Arboreal guenon species that inhabits the West African rain forest belt between
Gambia and Ghana.
Adults: alarm calls in response to eagles and leopards, their two main preys.
Striking sexual dimorphism in these alarm calls.
Video leopard

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StudyTaï National Park, Côte d’Ivoire, June 1994 – June 1997

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Group of 20 individuals, 1 fully adult male, several adult females with theiroffspring. 30 different groups probably studied.
Four different vocalizations used as playback:(a) 15s of grows of an African leopard(b) 15s of shrieks of a crowned eagle;(c) series of male diana monkey alarm calls in response to leopard;(d) series of male diana monkey alarm calls in response to eagle.

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Alarm calls played in series of five calls (in some cases three for the eagle call,which is longer).
Prior study:• Presentation of acoustic predator models provides reliable way ofstimulating predator presence.
• Acoustic responses to real leopards and to playbacks were identical. Samefor eagles.

Miyagawa July 201917Experimental design: prime – probe pairings
Playback of prime, followed 5 minutes later by probe. 5 min. because that theinterval after which behavior returns to baseline.
Baseline: prime and probe were alike:
Eagle shrieks, eagle shrieks
Test condition: only the semantic features were alike:Male’s eagle alarm call, eagle shrieks
Control condition: both the acoustic and semantic feature were different:
Male’s leopard alarm calls, eagle shrieks

Test for habituation

Miyagawa July 201918Miyagawa July 201919

Predictions:Baseline: habituation
Strong reaction to the prime, weak reaction to the probe
Test: habituation
Strong reaction to the prime, weak reaction to the probe
Control: nonhabituation
Strong reaction to both prime and probe
To avoid unwanted dependencies in the data, each group was tested only once.
89 playback trials, 31 could not be used (experimenter detected, predation
event, moved away)
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Results were as predicted, crucially for female diana monkeys.

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Old World Monkeys
Old World monkeys such as the Diana monkeys, Campbell’smonkeys, and De Brazza’s monkeys have what appear to be a
combinatorial system in which they can put together twoindependent items.

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What we will show, based on the analysis of the reported data, isthat these monkeys indeed have a way to create a two-term

expression. This is consistent with Fitch and Hauser’s finding thattamarins can learn AB sequences.

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Assuming this AB sequence to be associated with the frontal
operculum, this is also consistent with the observation that thefrontal operculum supports the combining of two elements insequence, rather than building a hierarchical structure

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System of Two: Putty-nosed monkey
Putty-nosed monkeys (Arnold and Zuberbühler 2012)pyow (=P) and hack=(H);Pyows function as general alert calls, whereas hacks are usually related
to aerial predators.
PPPHHH (can only be used for non-risk-related situations)
PHHHHH
PPPPHH*PHP…

“phonologically complex,
but lexically simple” (Schlenker 2016)

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Dual-compartment framepyownhackn

12

See Progovac (2015)

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Campbell’s monkeys
Ouattara et al. (2009)
The adult males of six wild Campbell’smonkey groups in the Tai Forest

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Affixation in the alarm calls of free-ranging adult
Campbell’s monkeys (Cercopithecus campbelli campbelli)Male alarm calls are composed of an acoustically variable stem,
which can be followed by an acoustically invariable suffix.
Suffixation functions to broaden the calls’ meaning by:(i) transforming a highly specific eagle alarm to a generalarboreal disturbance call;or(ii) by transforming a highly specific leopard alarm call to a
general alert call.

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Stems and an affix
The adult males consistently produced six different loud alarm calltypes:(a) boom(b) krak(c) hok(d) wak-oo(e) krak-oo(f) hok-oo

All were perceptually
distinct to a humanobserver.

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“Meaning” of Campbell alarm calls
krak : exclusively given after detecting a leopard, suggesting that it
functioned as a leopard alarm callkrak-oo : given to almost any disturbance, suggesting it functioned
as a general alert call.
hok : almost exclusively associated with the presence of a crowned
eagle (either a real eagle attack or in response to anothermonkey’s eagle alarm calls)

hok-oo : given to a range of disturbances within the canopy,
including the presence of an eagle or a neighboring group.

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On hok and hok-oo
On a few occasions, hok and hok-oo calls were produced in response
to a flying squirrel, whose silhouette somewhat resembles a flyingeagle, but never to any other large bird.
While producing hok-oo calls, males adopted a threat posture,
combined with flashing their eyelids, and they sometimes conducted ashort dash towards the disturbance.
Adding an oo unit to hok, thus, indicated that the male wasaggressively motivated -- in response to a general disturbance within
the canopy, e.g., a perched eagle or a conspecific opponent.

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Field experiments
To investigate the predator warning function more directly, aseries of field experiments were performed that simulated thepresence of the different predators, using both visual andacoustic models.

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Research question for us
Ouattara et al. (2009) (and Schlenker 2016) simply assume that-oo is affixed to krak (krak-oo) and hok- (hok-oo). But an equallyplausible view is that krak-oo and hok-oo are single lexical items andthe shape and meaning similarities are coincidental.

NOTE: wak-oo (similar in usage to hok-oo). *wak-To test to see if the Campbell’s monkeys actually detect the “root” inkrak-oo, we looked closely at the data presented by Ouattara et al.
(2009).
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Campbell’s Monkey data (Outtara et al. 2009)
Experiments with four conditions
krak-ookrak

hok-oohok151

Eaglevisual

91

37

Eagleacoustic

62

7 (3/7)

Leopardvisual

4 (1/7)273

Leopardacoustic

67

42 (4/7)
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9 (2/9)35

Campbell’s Monkey data (Outtara et al. 2009)
VISUAL PRESENTATION OF THE PREY
krak-ookrak

Eaglevisual

91

Leopardvisual

4 (1/7)hok-oo

hok37

151

273

Miyagawa July 201936Informativity Principle
When one call is strictly more informative than another, themost informative one is used whenever possible(Schlenker 2016: 18)
Revision:
When two alarm calls contain reference to the same predator,
the more informative one is used whenever possible.

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Hok, hok-oo
When presented with an eagle model:

hok (151), krak-oo (91)
But what about hok-oo (31)? Contradicts the revised
Informativity Principle?
hok-oo appears to have additional function beyond hok: ‘[w]hile
producing "hok-oo” calls, males adopted a threat posture,
combined with flashing their eyelids, and they sometimes
conducted a short dash towards the disturbance’ (Outtara 2009:3)."
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Recap: Campbell’s Monkey data (Outtara et al. 2009)
ACOUSTIC PRESENTATION
krak-ooEagleacoustic

62

Leopardacoustic

67

krak

hok-oo7 (3/7)hok9 (2/9)

42 (4/7)

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The asymmetry in the use of krak-oo for leopard vs. eaglesuggests that Campbell’s monkeys are aware that krak in krak-oo
carries the meaning of “leopard” despite the fact that krak-oo isa general alarm call.
This still does not answer the question, do the monkeys have an
operation of affixation, a form of Merge, or do they learn
krak-oo as a single expression?

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De Brazza’s monkeys
Bouchet et al. (2012) studied 23 De Brazza monkeys in captivity
that included three juvenile males, three juvenile females, fiveadult males, and 12 adult females, all captive-born. The inclusionof the juvenile monkeys allowed for developmental study ofcalls, which becomes important for our study.

Miyagawa July 201941Bouchet et al. (2012) report that the monkeys produced ten
distinct call types; we will focus on three of them, On, I, and OnI.
On calls occurred with gazes directed to the adult male by adultfemales as well as both sexes of juveniles. The adult male madethis call when gazing at zoo-keepers, the research observer, orneighboring groups.

I calls were uttered by juveniles when approaching the adultmale to establish physical contact.
OnI calls were made by adult females and juveniles of both sexes
when approaching a male but with ambivalence about whether
to approach or escape.

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Distribution of De Brazza’s monkey calls
FemalesJuveniles Adults
OnOnI
OnI
OnI

Males
Juveniles
AdultsOnOnI
OnI

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Conclusion• Primates have the ability to form two-item expressions, but never morethan two;• The formation of the two-item expression does not involve an operationsuch as Merge, thus it is a simple regular grammar;• The frontal operculum supports the combining of two elements insequence, rather than building a hierarchical structure (Zaccarella et al.

2015);• Monkeys have well-developed frontal operculum (Sanides 2019);• Human language is infinite, and this comes from the combinatorial
operation of Merge, which is located in the Broca’s area (Friederici et al.
2006, etc.), which is phylogenetically newer than the FOP.
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