Download Broca`s area and the evolution of language

Broca’s area
and the evolution of language
TOM SCHOENEMANN
Anthropology
Cognitive Science
Human Brain Evolution Lab
Stone Age Institute
Indiana University
Sunday, November 11, 12
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我很
幸被邀请，
因为我的普通话很好了，
所以接下来我要练习英语。
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How did language evolve?
Common view in linguistics: Language required
new, language-specific circuits
Alternative view: Language adapted to the human
brain
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Language evolution did require some brain
evolution
‣ Chimps don’t have the same linguistic abilities as
humans
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Co-evolution of brain and language
language
evolution
brain
evolution
other
behavioral
evolution
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Two evolutionary routes to a neural circuit
ancestral
condition
existing
circuit
new circuit
existing
circuit + A
existing
circuit + A + B
modern
condition
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new
circuit + Z
new
circuit + Z + Y
modern complex circuit
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The process of language evolution
ancestral state
population
lacking
language
?
??
???
population
using
language
current state
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In each generation:
‣ It must have been beneficial to use the most
sophisticated language possible
‣ Individuals were limited by the biology they were born
with: behavioral adaptation vs. genetic change
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It follows that...
‣ Language evolution is constrained by the limitations of
the brains that exist in each generation
‣ Language most likely evolves through the modification
of pre-existing brain circuitry
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Two evolutionary routes to a neural circuit
ancestral
condition
existing
circuit
new circuit
existing
circuit + A
existing
circuit + A + B
modern
condition
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new
circuit + Z
new
circuit + Z + Y
modern complex circuit
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Does the brain adapt to behavior, or
behavior adapt to the brain?
“Religious concepts and activities hijack our
cognitive resources, as do music, visual art,
cuisine, politics, economic institutions and
fashion.”
Pascal Boyer
2008
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What does a large brain allow?
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Evolution of hominin cranial capacity
Data from Holloway et al., 2004 and others
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Brain size and conceptual complexity
‣ Concepts are based upon complex networks
connecting different brain regions
‣ Size of cortical and subcortical areas are proportional to
the degree of elaboration of functions
‣ Increasing brain size is correlated with increasing
degree of specialization of parts of the brain
Schoenemann 2005, 2009, 2010, 2012
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Social group size vs. brain volume in primates
Hurst 2011
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Repertoire size vs. brain volume in primates
Hurst 2011
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Behavioral associations with brain volume
in primates
social group size
repertoire size
Hurst 2011
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Different brain regions evolved in
different ways
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Areas that have lagged behind...
Primary Motor!
~33%!
Premotor!
~60%!
Olfactory
bulb!
~30%!
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Primary
Visual!
~60%!
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Temporal lobe
Temporal
lobe!
~120%!
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Behavior mediated by temporal lobe
areas
• auditory processing
• forming long-term memories
• emotional assessment
• face recognition
• aspects of language, particularly: connecting
concepts to words
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Prefrontal cortex
Primary Motor!
Somatosensory!
Premotor!
Prefrontal!
Primary
Visual!
Primary Auditory!
Brainstem!
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Cerebellum!
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Areas of greatest expansion
Superior
Anterior
left lateral
Avants et al., (2006)
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Behavior mediated by prefrontal
cortical areas
• planning future behavior
• maintaining goals
• temporary storage/manipulation of information
(‘working memory’)
• memory for sequential order
• selective attention
• social information processing
• aspects of language, particularly: sequential
and semantic information processing
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Evolution of language areas
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Non-human primates have homologous
“language” areas
Striedter 2005
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Evolutionary elaboration of the connections
between Broca’s and Wernicke’s areas
Evolution of language areas
Rilling et al. 2008
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Total
6
Results of Spearman’s r
coordination task and o
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No asymmetry of Broca’s area in chimpanzees
2
Parameter
0
B
Left
Area 44
Right
Area 44
Left
Area 45
Right
Area 45
1200
Neuron number AQ 44
Neuron number AQ 45
Volume AQ 44
Volume AQ 45
Neuron density AQ 44
Neuron density AQ 45
Volume (cm3)
1000
800
600
400
200
0
C
Left
Area 44
Right
Area 44
Left
Area 45
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Schenker et al. 2010
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Right
Area 45
chimpanzees. U
ture and functio
a crucial com
characteristics
our common a
recent speciali
support linguist
There is sub
topographic ex
individuals and b
(Amunts et al. 1
zees also indica
homologue in c
have further do
areas 44 and 4
consistent with
29
Asymmetry of Broca’s area in humans
p<.001, fdr-corrected, N=72
Kitchell and Schoenemann in prep.
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Asymmetry of Broca’s area in humans
p<.001, fdr-corrected, N=72
Kitchell and Schoenemann in prep.
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Asymmetry of Broca’s area in humans
p<.001, fdr-corrected, N=72
Kitchell and Schoenemann in prep.
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Asymmetry of cerebellum in humans
p<.001, fdr-corrected, N=72
Kitchell and Schoenemann in prep.
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Asymmetry of Wernicke’s area in humans
p<.001, fdr-corrected, N=72
Kitchell and Schoenemann in prep.
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Are brain asymmetries reflected on
the inner surface of the skull?
brain
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endocast (“braincase”)
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Broca’s area
brain
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Broca’s cap
endocast (“braincase”)
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Asymmetry of the endocranial surface in apes
10%
Human
35%
Chimpanzee
Bonobo
Schoenemann et al. 2008
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Pan troglodytes morphed into Homo sapiens
left lateral
anterior
superior
right lateral
posterior
inferior
Schoenemann et al. 2011
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Can we trace the evolution of
Broca’s cap in the fossil record?
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Evidence of the evolution of broca’s area in
Homo erectus?
left hemisphere
right hemisphere
Broca’s cap on Sambungmacan 3
~300,000 years old
Broadfield et al. 2001
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What is the evolutionary history of Broca’s cap
asymmetry?
extant H. sapiens
1800
1600
1400
A. afarensis
A. ethiopicus
A. boisei
A. robustus
A. africanus
1200
Cranial Capacity (cc)
Ardipithecus ramidus
A. garhi
H. habilis
1000
H. ergaster
H. rudolfensis
H. georgicus
800
H. erectus
H. antecessor
H. soloensis
Pan troglodytes
600
400
200
H. heidelbergensis
H. sapiens neanderthalensis
H. sapiens idaltu
H. sapiens sapiens
H. floresiensis
Pan troglodytes
extant H. sapiens
0
5.0
4.0
3.0
2.0
Millions of Years Ago
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1.0
0.0
Data from Holloway et al., 2004 and others
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right lateral
left lateral
Fossils are often incomplete in
the region of Broca’s cap
周口店 Zhoukoudian
~600,000 - 400,000 years old
Wu et al. 2010
Fig. 3. From left to right: superior, frontal, right lateral, left lateral and posterior views of the six ZKD endocasts. They are in chronological order with the geo
V, in the bottom row. A1–A5: ZKD III; B1–B5: ZKD II; C1–C5: ZKD X; D1–D5: ZKD XI; E1–E5: ZKD XII; F1–F5: ZKD V.
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Evolution of asymmetrical Broca’s cap
extant H. sapiens
1800
1600
1400
A. afarensis
A. ethiopicus
A. boisei
A. robustus
A. africanus
1200
Cranial Capacity (cc)
Ardipithecus ramidus
A. garhi
H. habilis
1000
H. ergaster
H. rudolfensis
H. georgicus
800
H. erectus
H. antecessor
H. soloensis
Pan troglodytes
600
400
200
H. heidelbergensis
H. sapiens neanderthalensis
H. sapiens idaltu
H. sapiens sapiens
H. floresiensis
Pan troglodytes
extant H. sapiens
0
5.0
4.0
3.0
2.0
Millions of Years Ago
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1.0
0.0
Data from Holloway et al., 2004 and others
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Evolution of asymmetrical Broca’s cap
1800
1600
extant H. sapiens
right-biased
1400
A. africanus
A. ethiopicus
H. rudolfensis
H. ergaster
H. erectus
H. heidelbergensis
1200
Cranial Capacity (cc)
H. soloensis
H. sapiens neanderthalensis
1000
Pan troglodytes
extant H. sapiens
800
no asymmetry
Pan troglodytes
600
400
200
0
5.0
4.0
3.0
2.0
Millions of Years Ago
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1.0
0.0
Data from Holloway et al., 2004 and others
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Evolution of left-biased Broca’s cap
1600
周口店 Zhoukoudian III, E (Z 2)
1400
and Sambungmacan 3
1200
extant H. sapiens
1800
A. africanus
A. ethiopicus
H. rudolfensis
H. ergaster
H. erectus
H. heidelbergensis
Cranial Capacity (cc)
H. soloensis
H. sapiens neanderthalensis
1000
Pan troglodytes
extant H. sapiens
800
Pan troglodytes
600
400
200
0
5.0
4.0
3.0
2.0
Millions of Years Ago
Sunday, November 11, 12
1.0
0.0
Data from Holloway et al., 2004 and others
45
Evidence of the evolution of broca’s area in
Homo erectus?
Broca’s cap on Sambungmacan 3
Broadfield et al. 2001
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Evolution of left-biased Broca’s cap
extant H. sapiens
1800
1600
1400
A. africanus
A. ethiopicus
H. rudolfensis
H. ergaster
H. erectus
H. heidelbergensis
1200
Cranial Capacity (cc)
H. soloensis
H. sapiens neanderthalensis
1000
Pan troglodytes
extant H. sapiens
KNM-ER 1470
800
Pan troglodytes
600
400
200
0
5.0
4.0
3.0
2.0
Millions of Years Ago
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1.0
0.0
Data from Holloway et al., 2004 and others
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Evidence of the evolution of Broca’s area in
Homo habilis?
KNM ER 1470
brain endocast
~1.8 MYA
orangutan
chimpanzee
gorilla
human
Falk 1983
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Reading behavior into fossil endocasts
aim.uzh.ch
Scientificdevelopments.com
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Can we bypass the brain?
aim.uzh.ch
http://muskingum.edu/~neuro/neurpage/brains.htm
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Repertoire size vs. brain volume in primates
Hurst 2011
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Does endocranial shape correlate with vocal
repertoire size across primates?
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left lateral
anterior
superior
right lateral
posterior
inferior
52
Does endocranial shape predict
anything about the number of
vocalizations a primate species uses?
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Correlation between endocranial surface shape
and vocal repertoire size in primates
left lateral
anterior
superior
Broca’s cap
N=25
posterior
right lateral
inferior
Hurst et al. 2011
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Why does Broca’s area process language?
Two perspectives:
• Language needs particular types of processing, so these
areas exist (evolved) to fill this need
• These areas originally processed information in ways that
happen to be useful to language behavior - language
adapted to them
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Predictions:
• Non-linguistic - but potentially language-useful -
processing occurs in language area homologs in nonhuman primates
• ‘Language’ areas in humans retain these same nonlinguistic, ‘language-useful’ functions
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What does Broca’s area mediate in
non-linguistic primates?
• species-specific calls (Gil-da-Costa et al. 2006)
• orofacial motor sequencing (Petrides et al.
2005)
• active controlled retrieval of visual object and
spatial information (Petrides and Pandya 2009)
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Non-linguistic processing in
human Broca’s area?
• Sequential pattern recognition/processing/learning
(Christiansen & Ellefson 2002; Petersson et al. 2004)
• Detection of tone changes (Müller et al. 2001)
• Imagining hand motions (Binkofski et al. 2000)
Do non-human primates activate Broca’s
area when doing non-linguistic tasks?
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Two different possible outcomes in
non-human primate brains:
• Broca’s areas is activated: language processing
hijacked pre-existing circuitry
• Broca’s area is NOT activated: non-human primates
accomplish the same task using other circuits (...what
DID Broca’s area evolve for?)
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How can we test for sequential rule
learning in non-human primates?
• artificial grammar learning
• implicit learning
• serial reaction time
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. The participants were instructed to read the sentences carefully and attentively
ehension and to indicate for each sentence whether or not it was acceptable. Before the FM
A simple grammar
ment started, each subject practiced on practice sentences to familiarize with the experime
ure. The experimental sentences were presented in 4 blocks of approximately 10 minu
with a short break between each block.
#
S
V
M
S
#
X
R
M
V
X
R
(Petersson et al. 2004)
2:Sunday,
TheNovember
finite-state
architecture parsing and producing the simple right-linear unification grammar used61in
11, 12
Stimulus pictures used (for human version)
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[at the end of the sequence, a tone sounds]
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Example human subject
mean(reac%on(%me(
450#
reac%on(%me((ms)(
400#
p<.0001#
vs.#test1#
gramma0cal#
350#
300#
250#
200#
1#
2#
3#
4#
Test1#
Test1#
gramma0cal# ungramma0cal#
Block(
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Goals of the study
Within humans:
• What is the functional overlap of
• non-linguistic implicit grammar learning
• natural language grammar
Within apes (and other species):
• Does non-linquistic implicit grammar learning occur?
• If so, is Broca’s area involved?
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Summary
• Modifying pre-existing brain circuitry is always the most
likely evolutionary scenario
• Brain size in primates is associated with both:
1) richness of vocalizations
2) size of social group (and presumably social
complexity)
• Parts of the brain relevant to language have undergone
disproportionate expansion during evolution
• Broca’s area is asymmetric (left > right) in humans but not
apes
• Broca’s cap asymmetry is very old in human evolution
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Summary
• Broca’s area may have evolved to extract any kind of
sequential pattern information from the enviroment
• This would have made it a useful substrate for language to
utilize
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Acknowledgements:
Indiana University:
Dr. Nicholas Toth, Dr. Kathy Shick, Del Hurst, Mackenzie Loyet, Robert Mahaney
Indianapolis Zoo:
Dr. Robert Shumaker
University of California, Berkeley:
Vincent Sarich, William S-Y. Wang
University of Michigan-Dearborn:
Nida Syed
University of Pennsylvania:
Dr. James Gee, Dr. Brian Avants, Dr. Janet Monge, Dr. Murray Grossman, Daniel
Glotzer, Michael Sheehan, Jason Lewis
Yerkes Regional Primate Research Center:
Dr. Lisa Parr, Dr. James Rilling, Dr. Thomas Insel
Center for Functional Imaging, Lawrence Berkeley National Laboratory:
Dr. Thomas Budinger, Dr. Xia Teng, Dr. Sundar Amartur, Babak Razani, Yenchi
Wang, Mary Vasquez, Catherine Pham
Magnetic Resonance Science Center, University of California, San Francisco:
Dr. Sarah Nelson, Gary Ciciriello, Margaret Lobo, Evelyn Proctor, Niles Bruce
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