Putting neurons in culture:

The cerebral foundations of

reading and mathematics

III. The human Turing

machine
Stanislas Dehaene

Collge de France,
and
INSERM-CEA Cognitive Neuroimaging Unit
NeuroSpin Center, Saclay, France
Raoul Hausmann. L'esprit de notre time (Tte mcanique)
Paris, Muse National dArt Moderne

Summary of preceding talks:

The brain mechanisms of reading
and elementary arithmetic
Human cultural inventions are based
on the recycling (or reconversion) of
elementary neuronal mechanisms
inherited from our evolution, and
whose function is sufficiently close to
the new one.
Why are we the only primates capable
of cultural invention?

quantity
representation

high-level
control
verbal
code

visual
form

A classical solution: new modules

unique to the human brain
Michael Tomasello (The cultural origins of human cognition, 2000)
Human beings are biologically adapted for culture in ways that other primates
are not. The difference can be clearly seen when the social learning skills of
humans and their nearest primate relatives are systematically compared. The
human adaptation for culture begins to make itself manifest in human
ontogeny at around 1 year of age as human infants come to understand other
persons as intentional agents like the self and so engage in joint attentional
interactions with them. This understanding then enables young children to
employ some uniquely powerful forms of cultural learning to acquire the
accumulated wisdom of their cultures
Theory of mind and language abilities certainly play an important role in
our species pedagogical abilities, and therefore the transmission of culture
However, they do not begin to explain our remarkably flexible ability for
cultural invention cutting across almost all cognitive domains. Another
design feature is needed.

The theory of a global workspace

In addition to the processors that we inherited from our primate evolution,
the human brain may possess a well-developed non-modular global
workspace system, primarily relying on neurons with long-distance axons
particular dense in prefrontal and parietal cortices
Thanks to this system,
- processors that do not typically communicate with one another can
exchange information
- information can be accumulated across time and across different processors
- we can discretize incoming information arising from analog statistical inputs
- we can perform chains of operations and branching
The resulting operation may (superficially) resemble the operation of a
rudimentary Turing machine

The Turing machine:

a theoretical model of mathematical operations
Turing, A. M. (1936). On computable numbers, with an application to the Entscheidungsproblem. Proc. London Math. Soc., 42(230-265).

m-configurations
S(r)

scanned
square
a
t
a

qn

We may compare a man in the process of computing a real number to

a machine which is only capable of a finite number of conditions q1,
q2, qR which will be called m-configurations .
The machine is supplied with a tape (the analogue of paper) running
through it, and divided into sections (called squares ) each capable of
bearing a symbol .
At any moment, there is just one square, say the r-th, bearing the
symbol S(r), which is in the machine . We may call this square the
scanned square . The symbol on the scanned square may be called
the scanned symbol . The scanned symbol is the only one of
which the machine is, so to speak, directly aware . (...)
The possible behaviour of the machine at any moment is determined by
the m-configuration qn and the scanned symbol S(r). [This behaviour is
limited to writing or deleting a symbol, changing the m-configuration,
or moving the tape.]
It is my contention that these operations include all those which are
used in the computation of a number.

Infinite tape

The essential features of the Turing machine

Turing makes a number of postulates concerning the human brain.
Mental objects are discrete and symbolic
At a given moment, only a single mental object is in awareness
There is a limited set of elementary operations (which operate
without awareness)
Other mental operations are achieved through the conscious
execution of a series of elementary operations (a serial algorithm)

m-configurations
S(r)

scanned
square
d
a
t
a

The Church-Turing thesis:

Any function that can be computed by a human being can be
computed by a Turing machine

qn

Infinite tape

During his career, Turing himself kept a distanced attitude with this thesis :
On the one hand, he attempted to design the first artificial intelligence programs (e.g.
the first Chess program) and suggested that the behavior of a computer might be
indistinguishable from that of a human being (Turing test).
On the other, he did not exclude that the human brain may possess intuitions (as
opposed to mere computing ingenuity) and envisaged an oracle-machine that would
be more powerful that a Turing machine

The fate of the computer metaphor

in cognitive science and neuroscience
The concepts of Turing machine and of information processing have played a
key role at the inception of cognitive science
Since the sixties, cognitive psychology has tried to define the algorithms used by
the human brain to read, calculate, search in memory, etc.
Some researchers and philosophers even envisaged that the brain-computer
metaphor was the final metaphor that need never be supplanted, given that
the physical nature [of the brain] places no constraints on the pattern of thought
(Johnson-Laird, Mental models, 1983)
However, the computer metaphor turned out to be unsatisfactory:
The most elementary operations of the human brain, such as face recognition
or speaker-invariant speech recognition, were the most difficult to capture by a
computer algorithm
Conversely, the most difficult operations for a human brain, such as computing
357x456, were the easiest for the computer.

The human brain:

A massively parallel machine
~1011 neurons
~10

15

synapses

For basic perceptual and motor operations,

computing with networks and attractors
provides a strong alternative to the computer metaphor
- Mental objects are coded as graded activation levels, not discrete symbols
-Computation is massively parallel

Model of written word recognition

(McClelland and Rumelhart, 1981)
Model of face recognition
(Shimon Ullman)

Even mathematical operations the very domain that inspired Turing

do not seem to operate according to classical computer algorithms
The Distance Effect in number comparison
(first discovered by Moyer and Landauer, 1967)

800

99
31

Response time
750
700

84
52

650
600

larger or
smaller
than 65 ?

550
500
450

smaller

larger

400
30

0.2

Error rate

40

0.1

50

60

70

80

90

0
100

Target numbers
Dehaene, S., Dupoux, E., & Mehler, J. (1990). Journal of Experimental Psychology: Human Perception and Performance, 16, 626-641.

Do Turing-like operations bear no relation

to the operations of the human brain?
This conclusion seems paradoxical, given the wide acceptance of the ChurchTuring thesis in mathematics.
However...
When we perform complex calculations, our response time is well predicted
by the sum of the durations of each elementary operation, with appropriate
branching points
In some tasks that require a conscious effort, the human brain operates as a
very slow serial machine.
In spite of its parallel architecture, it presents a central stage during which
mental operations only operate sequentially.

On the impossibility of executing two tasks at once

Response time

The psychological refractory period

(Welford, 1952; Pashler, 1984)
Response
2

Response
1
Task 2
Task 1
Target T1

Response
2
Target T2
2

Target T2

time

Response
1

Time interval between stimuli

On the impossibility of executing two tasks at once

Response time

The psychological refractory period

(Welford, 1952; Pashler, 1984)
Response
2

Response
1
Task 2
Task 1
Target T1

Response
2
Target T2

Target T2

time

Response
1

Time interval between stimuli

On the impossibility of executing two tasks at once

Response time

The psychological refractory period

(Welford, 1952; Pashler, 1984)
Response
2

Response
1

Response
2

Task 2
Task 1
Target T1

Target T2

Target T2

time

Response
1

Time interval between stimuli

On the impossibility of executing two tasks at once

Response time

The psychological refractory period

(Welford, 1952; Pashler, 1984)
Response
1

Response
2

Response
2

Task 2
Task 1
Target T1

Target T2

Target T2

time

Response
1

Time interval between stimuli

On the impossibility of executing two tasks at once

Response time

The psychological refractory period

(Welford, 1952; Pashler, 1984)
Response
1

Response
2

Response
2

Task 2
Task 1
Stimuli 1 et 2

Target T2

time

Response
1

Time interval between stimuli

On the impossibility of executing two tasks at once

Response time

Pashler (1984) :
-only central operations are serial
- perceptual and motor stages run in parallel

slack time
P2
P1

Response
1
C2

C1

Stimuli 1 and 2

Target T1

Response
2

Response
2
M2

Slowing the P stage

by presenting
numerals in Arabic
or in verbal notation

Target T2
2

Task 2
Response
1

M1 Task 1
time

Response 1
Time interval between stimuli

Target T2

Response 2
Sigman and Dehaene, PLOS Biology, 2005

Event-related potentials dissociate parallel and serial

stages during dual-task processing
Subjects were engaged in a
dual-task:
-number comparison of a visual
Arabic numeral with 45,
respond with right hand
-followed by pitch judgment on
an auditory tone, respond with
left hand
2.5

1800

Response times

1400

RT2

1000

RT1
600
0

300

900

1200

T1-T2 delay

Separation of ERPs at long T1-T2 delays

1.5

1
0.5
0
-1000

-500

N1

500

P3

Visual events

1000

N1

1500

2000

P3

Auditory events

Sigman and Dehaene, in preparation

Event-related potentials dissociate parallel and serial

stages during dual-task processing
Subjects were engaged in a
dual-task:
-number comparison of a visual
Arabic numeral with 45,
respond with right hand

1800

Response times

1.5
1
0.5

1400

RT2

N1

-0 . 5
-1
-5 0 0

1000

500

1000

1500

500

1000

1500

500

1000

1500

500

1000

1500

1.5

-followed by pitch judgment on

an auditory tone, respond with
left hand
2.5

RT1

600

0.5

300

900

T1-T2 delay

1200 P3

0
-0 . 5
-5 0 0

Separation of ERPs at long T1-T2 delays

1.5

1.5

1
0.5

N1

0.5
0
-1000

-0 . 5
-1
-5 0 0

-500

500

1000

1500

2000
1.5
1
0.5
0

N1

P3

Visual events

N1

P3

Auditory events

P3

-0 . 5
-1
-5 0 0

Sigman and Dehaene, in preparation

Locating the sites of processing bottlenecks:

parieto-prefrontal networks

Dux, Ivanoff, Asplund & Marois, Neuron, 2007

PRP
VSTM/MOT
Att. Blink

Marois & Ivanoff, TICS, 2005

review of imaging studies of bottleneck tasks

The central stage is associated with conscious processing

The attentional blink phenomenon
When both T1 and T2 are briefly presented and
followed by a maks, participants who perform a
task on T1 may fail to report or even perceive
the presence of T2.
P2
P1

C1

Percentage of perceived stimuli

C2

M2

M1 Task 1

Target T1 Target T2 (masked)

Time interval between stimuli

J. Raymond, K. Shapiro, J. Duncan, C. Sergent

Conscious access and non-conscious processing

during the attentional blink
Variable T1-T2 lag
Target
1

Target 2

HRQF
CINQ
CVGR

XOOX

time

90

Percent of trials

Bimodal
distribution of T2 visibility
80
Seen
70
60
50

Not seen

40
30
20
10
0
1

T1-T2Lag
Lag

10

12

14

y ibrat
t
i
l
i
b
i
u is
SV
6

is
ive v
bject

16

18

20

ing

ility

Sergent, Baillet & Dehaene, Nature Neuroscience, 2005

Time course of scalp-recorded potentials

during the attentional blink
UNSEEN T2
SEEN T2
(minus T2-absent trials) (minus T2-absent trials)

DIFFERENCE

Sergent et al., Nature Neuroscience, 2005

Timing the divergence between seen and not-seen trials

in the attentional blink (Sergent et al., Nature Neuroscience 2005)
Unchanged initial processing

Late non-conscious processing

P1 : 96 ms

N1 : 180 ms

N4 : 348 ms

-2 V

-4 V

-3 V

Seen

Not seen

+2 V

+4 V

Abrupt divergence around 270 ms

N2 : 276 ms

N3 : 300 ms

-2 V

-3 V

+3 V

All-or-none ignition
P3a : 436 ms

P3b : 576 ms

Seen

Not seen

+2 V

+3 V

-2 V

+2 V

-2 V

+2 V

The cerebral mechanisms of this central limitation:

a collision of the N2 and P3 waves
PROCESSING OF TASK 1 (difference task/no task)

N2

P3a

P3b

+3 V
-3 V

T1
onset

100
-200

200
-100

300

400
100

T2
onset

500
200

600
300

700
400

800
500

time from T1
onset (ms)
time from T2
onset (ms)

+2 V
-2 V

N2

P3a

P3b

PROCESSING OF TASK 2 (difference seen/not seen)

Dehaene, Baillet et Sergent, Nature Neuroscience 2005

Sources of the difference between seen and unseen trials

Middle temporal

t = 300 ms

seen
not seen
Inferior frontal

seen
not seen
absent

Dorsolateral prefrontal

t = 436 ms

Activation in event-related potentials:

Sergent, Baillet & Dehaene, Nature Neuroscience, 2005

fMRI activation to a seen or unseen

stimulus during the attentional blink
Marois et al., Neuron 2004

Sources of the difference between seen and unseen trials

Middle temporal

t = 300 ms

seen
not seen
Inferior frontal

Dorsolateral prefrontal

t = 436 ms

Activation in event-related potentials:

Sergent, Baillet & Dehaene, Nature Neuroscience, 2005

Phase synchrony in MEG:

Gross et al, PNAS 2004

An architecture mixing parallel and serial processing:

Baars (1989) theory of a conscious global workspace

The global neuronal workspace model

(Dehaene & Changeux)

hierarchy of modular
processors

automatically
activated
processors

high-level processors
with strong
long-distance
interconnectivity

processors
mobilized
into the
conscious
workspace

Dehaene, Kerszberg & Changeux, PNAS, 1998

Dehaene & Changeux, PNAS, 2003; PLOS, 2005
inspired by Mesulam, Brain, 1998

Prefrontal cortex and temporo-parietal association areas

form long-distance networks
Von Economo (1929):
Greater layer II/III thickness

Guy Elston (2000)

Greater arborizations and spine density

V1

TE
Pat Goldman-Rakic
(1980s):
long-distance
connectivity of dorsolateral prefrontal cortex

PFC

Detailed simulations of the global neuronal workspace

using a semi-realistic network of spiking neurons
(Dehaene et al., PNAS 2003, PLOS Biology, 2005)
Area D

Area C
Area B1

Area B2

Area A1

Area A2

Feedforward

T1

T2

60
40
20
0

Feedback
Thalamocortical column

Spiking neurons

Cortex
supragranular

AMPA
NMDA

layer IV

GABA
neuromodulator
current

infragranular

to/from
lower
areas

to/from
higher
areas

NaP

Leak

Ignition of
the global
workspace by
target T1

100

200

300

400

500

Failure of
ignition by
target T2

Spike-rate
adaptation

KS
Optional cellular oscillator currents

Dehaene, Sergent, & Changeux, PNAS, 2003

Thalamus

Is the brain an analogical or a discrete machine?

A problem raised by John Von Neumann
Turing assumed that his machine processed discrete symbols
According to Von Neumann, there is a good reason for computing with discrete symbols, and
it also applies to the brain:
All experience with computing machines shows that if a computing machine has to handle as
complicated arithmetical tasks as the nervous system obviously must, facilities for rather high
levels of precision must be provided. The reason is that calculations are likely to be long, and in
the course of long calculations, not only do errors add up but also those committed early in the
calculation are amplified by the latter parts of it ()
Whatever the system is, it cannot fail to differ considerably from what we consciously and
explicitly consider as mathematics (The computer and the brain, 1958)

Why and how does the brain discretize incoming analog inputs?
The answer given by... Alan Turing
The decision algorithm by stochastic accumulation designed by Turing at Bletchley Park

probabilit y of I if A is true
Weight of input I in favor of A = Log

probabilit y of I if A is false
Total weight in favor of A = initial bias + weight ( I1 ) + weight ( I 2 ) + weight ( I 3 ) + ...
Evolution of the
weight in favor of A

Decision
boundary for A

Emission of
response A

Decision
boundary for non-A

From numerosity detectors to

numerical decisions:
Elements of a mathematical
theory
(S. Dehaene, Attention & Performance,
2006, in press)

1. Coding by Log-Gaussian numerosity detectors

1

16

Internal logarithmic scale : log(n)

2. Application of a criterion and formation of two pools of units

Criterion c

Stimulus of numerosity n

Pool favoring R1

Pool favoring R2

3. Computation of log-likelihood ratio by differencing

Pool favoring R2
Pool favoring R1

Response in simple arithmetic tasks:

-Larger or smaller than x?
-Equal to x?

LLR for R2 over R1

4. Accumulation of LLR, forming a random-walk process

Mean Response Time
Trial 1

Trial 2

Trial 3

Decision
threshold for R2

Starting
point of
accumulation
Decision
threshold for R1
Time

A fronto-parietal network might implement stochastic accumulation

Neurons in prefrontal and parietal
cortex exhibit a slow stochastic
increase in firing rate during
decision making

Stochastic accumulation can be

modeled by networks of selfconnected and competing neurons

Decision
Fixed threshold
Accumulation
at a
variable
speed

Simulated neuronal activity:

Wong & Wang, 2006

Kim & Shadlen, 1999

Hypothesis: there is an identity between the stochastic

accumulation system postulated in
and the central system postulated in PRP models
Task 1
Stimulus 1

The accumulation of evidence

required by Turings algorithm
would be implemented by the
recurrent connectivity of a
distributed parieto-frontal
system.

Response 1

RT1 Distribution

Task 2
Stimulus 2

P W

M
C

Response 2

RT2 Distribution

1000

2000

ms
Perceptual stage (P)

Central Integration (C)

Wait period (W)

Motor stage (M)

Sigman and Dehaene (PLoS 2005, PLoS 2006)

Is a stochastic random walk constitutive of the central stage ?

M

This model makes very specific predictions about

the source of variability in response time:
-

Factors that affect the P or M stages should

add a fixed delay
number notation (digits or words)
Motor complexity (one or two taps)

Factors that affect C should

increase variance
Numerical distance

Target T2

Response

RT Distribution

Perceptual stage (P)

Central Integration (C)
Motor stage (M)

C
factor
C
factor

P factor

M factor

P factor

M factor
Sigman & Dehaene, PLOS: Biology, 2004

Prefrontal and parietal cortices may contain a general

mechanism for creating discrete categorical representations

Categorical representation of visual

stimuli in the primate prefrontal cortex
(Freedman, Riesenhuber, Poggio & Miller,
Science, 2001).

Parietal representations can also be

categorical (Freedman & Assad, Nature 2006)
Whereas the rest of cortex can be characterized
as a fundamentally analog system operating on
graded, distributed information, the prefrontal
cortex has a more discrete, digital character.
(OReilly, Science 2006)

Exploring the cerebral mechanisms

of the non-linear threshold in conscious access
(Del Cul and Dehaene, submitted)

E
M6 M
+ E

Time

mask

Subjective visibility

Objective performance

+
.
.

6
+

Delay: 0-150ms

prime
16ms

delay

Logic = Use this sigmoidal profile as a signature of

conscious access. Which ERP components show this
profile?

Left target

1.5

100

80

60

40
100ms

1
0
-1

P1a
0.5

20

50

100

-3
-5
-6

16 33 50 66 83100

150

-2
-4

-Only the P3 shows a

non-linearity similar to
behavioral report

Amplitude

120

-Activation profiles
become increasingly
non-linear with time

Latency

1.5
100

P1b
140ms

1
0.5

50
0

50

100

120

1.5

N1

100
167ms
80
60
0

50

0.5
100

16 33 50 66 83100

240
220

200

N2

227ms

180

16 33 50 66 83100

180
160
140

160
140

50

100

16 33 50 66 83100

400

4
350

P3

300
370ms
0

50

1
100

16 33 50 66 83100

A late non-linearity underlying conscious access during masking

(Del Cul et Dehaene, submitted)

Delay:

Variable
delay
9

E
M M
E
16 ms

250 ms

Parietal

First phase:
local and linear

100 ms
83 ms
66 ms
50 ms
33 ms
16 ms

Second phase:
global and non-linear
(amplification)
Frontal

Fusiform

A hypothetical scheme for the human Turing machine

The workspace can perform complex, consciously controlled operations by
chaining several elementary steps
Each step consists in the top-down recruitment, by a fronto-parietal network, of a
set of specialized processors, and the slow accumulation of their inputs into
categorical bins, which allows to reach a conscious decision with a fixed,
predefined degree of accuracy.

time

Sigman & Dehaene, PLOS:Biology, 2005

Consciousness is needed for chaining of two operations

(Sackur and Dehaene, submitted)

Presentation of a masked digit (2, 4, 6, ou 8) just below threshold

Four tasks
Naming

Arithmetic

Comparison

Composite task

(example: n+2)

n+2

Subliminal Performance
on non-conscious trials

smaller

larger

Comparison
Naming

compare
smaller

larger

Arithmetic
Composite task (incongruent trials)

Chance level

Conclusions
Turing proposed a minimal model of how mathematical operations unfold in the
mathematicians brain
We now know that the Turing machine is not a good description of the overall
operation of our most basic processors
However, it might be a good description of the (highly restricted) level of serial
and conscious operations, which occur within a global neuronal workspace
The global neuronal workspace may have evolved to
- achieve discrete decisions by implementing Turings stochastic accumulation
algorithm on a global brain scale
- broadcast the resulting decision to other processors, thus allowing for serial
processing chains and a human Turing machine
- thus giving us access to new computational abilities (the ecological niche of
Turing-like recursive functions)
By allowing the top-down recruitment of specific processors, the global
workspace may play an important role in our cultural ability to play with our
modules and to invent novel uses for evolutionary ancient mechanisms
Very little is know about the human Turing machine:
- How does the brain represent and manipulate discrete symbols?
- What is the repertoire of elementary non-conscious operations?
- How do we pipe the result of one operation into another?