Mapping the Matrix: The Ways of Neocortex
Rodney J. Douglas1,* and Kevan A.C. Martin1,*
1Institute of Neuroinformatics, UZH/ETH, Winterthurerstrasse 190, 8057 Zurich, Switzerland
*Correspondence: email@example.com (R.J.D.), firstname.lastname@example.org (K.A.C.M.)
While we know that the neocortex occupies 85% of our brains and that its circuits allow an enormous
flexibility and repertoire of behavior (not to mention unexplained phenomena like consciousness),
a century after Cajal we have very little knowledge of the details of the cortical circuits or their
mode of function. One simplifying hypothesis that has existed since Cajal is that the neocortex con-
sists of repeated copies of the same fundamental circuit. However, finding that fundamental circuit
has proved elusive, although partial drafts of a ‘‘canonical circuit’’ appear in many different guises
of structure and function. Here, we review some critical stages in the history of this quest. In doing
so, we consider the style of cortical computation in relation to the neuronal machinery that supports
it. We conclude that the structure and function of cortex honors two major computational principles:
‘‘just-enough’’ and ‘‘just-in-time.’’
Maps are comforting. They reveal to us the fixed points
of the known world and alert us to the regions that are
‘‘terra incognita.’’ However, maps themselves also map
the changes in our perception of what is the ‘‘known
world’’—and these reveal our perceptions to be unstable.
was first ‘‘discovered’’ in 1578 somewhere between Ire-
land and Frisland and appeared on nautical charts from
then on until it finally sank from consciousness after it last
appeared on a chart in 1856. The island of Madya was the
longest survivor of these phantoms. It first appeared on
maps in about 1400, positioned in the north Atlantic to the
southwest of Ireland. Over the centuries it moved more
westward, so that by 1566 it was located near Newfound-
land, and then took a turn south, and was last seen on a
Rand McNally map of 1906 at the level of the West Indies.
Claude Levi-Strauss (in contrast to William of Occam: ‘‘No
more things should be presumed to exist than are abso-
lutely necessary’’) argued that every culture has a need
for certain concepts and expressions to absorb any ex-
cess of existence that has not yet had a word coined for
it. James Hamilton Paterson (1993) suggests that these
void of ignorance—the terra incognita.
The neocortex is one of the most elaborate maps we
have. Not only does it contain many different areas, but
these areas also contain within themselves multiple maps,
which may reflect directly the sensory periphery or may
has its own floating signifiers, with words like ‘‘column,’’
‘‘module,’’ ‘‘neural representation,’’ ‘‘cortical code,’’ and
‘‘consciousness,’’ which have been coined to absorb the
enormous functional and structural excess of existence
that is evident in every material record of the brain and,
most particularly, in the cortical circuits about whose
mode of organization and operation we are still greatly
ignorant. One fundamental question is whether the neo-
cortex is a unitary structure with a grammar and a logic
of construction and operation that can be understood
in terms of the physical circuits and their physiology, or
whether it is a collective of very many separate modules
with their own specialist ‘‘trick’’ circuitry?
The Languages of Neocortex
To begin at the beginning: like the syntax of human lan-
guages, the structure of the neocortex appears equally
complex in all land mammals. Just as there is no simple
or prototype version of a human language in existence, a
simple or primitive form of neocortex does not exist. Yet,
it is as evident that, like different languages, the neocortex
physiological methods. But just as with languages, we will
claim here, the neocortical areas are also essentially the
same and, like languages, can be translated, one into the
other. Thus, in understanding one area, we can expect to
a ‘‘canonical’’ property of cortical circuits (Douglas et al.,
1989). The immediate challenge is the question, what
defines ‘‘neocortex’’? The usual answer is structural:
genetically older, the neocortex possesses six layers. The
number of layers would, of course, seem a rather fragile
means of defining a structure that varies over five orders
the processing of input from an unlikely range of sensory
systems allowing detection of electromagnetic radiation,
vibration, temperature, sound, and chemicals, and that
then provides output to an equally unlikely range of motor
run. In fact, the ‘‘six-layered’’ neocortex is something of a
unicorn, for the number of layers that can be distinguished
varies greatly between areas and the histological stains
used to reveal the layers. Yet, somehow, neocortex is so
instantly distinguishable from other laminated structures,
Neuron 56, October 25, 2007 ª2007 Elsevier Inc.
such as the hippocampus or superior colliculus, that early
anatomists referred to it as ‘‘isocortex.’’
Although it is now clear that language comprehension
and production involves much more of the brain than just
the well-known regions first discovered by Broca and
Wernicke, their 19th century idea of a compartmentaliza-
tion of specific functions has reappeared in modern times,
most prominently in evolutionary biology. The best known
claim is captured by the ‘‘Swiss army knife’’ metaphor for
the functional organization of cortex (Barkow et al., 1992).
In this view, the brain has evolved a series of special-pur-
pose modules, which, like the Swiss army knife, consist of
individual components that have a specific function and
are not designed to work together like the components
of a machine. For humans, the language module is the
most obvious of these special-purpose modules, but
ules are the means by which the neocortex is organized
and works (Fodor, 1983; Zeki, 1993). Implicit in this is the
notion that the neural pathways in the brain subserving
eral-purpose architecture that carries out the neocortical
part of the computations.
Written on the Brain (in Indian Ink)
The era of microcircuit analysis was launched by Camillo
Golgi’s discovery of ‘‘la reazione nera,’’ which allowed in-
dividual neurons to be visualized, and by Santiago Ramon
y Cajal’s law of dynamic polarization, which provided the
critical algorithm for identifying the input and output
regions of individual neurons. Put together, these two
advances made it possible for the first time to show the
probable route of impulses from input to output for a given
structure. As he recorded in his autobiography, the ex-
traordinary claim that Cajal made was that even the high-
est center of the brain, the neocortex, was built of stereo-
typed circuits like those he had discovered in the retina,
cerebellum, hippocampus, spinal cord, and other parts of
the central nervous system (Cajal, 1937). Despite intense
efforts on his part, however, he was unable to define the
basic cortical circuit, but until the end of his life he never-
theless remained convinced that it existed.
When Cajal applied Golgi’s stain to neonatal brain, he
was able to map, mostly correctly, significant circuits in
the spinal cord, retina, and visual pathways, cerebellum,
hippocampus, olfactory bulb, auditory nuclei, and others.
From this he developed the notion of the ‘‘neural ava-
lanche,’’ which was essentially the inverse of Sherring-
ton’s ‘‘final common path.’’ It stated that the number of
neurons involved in conducting impulses from a sensory
receptor increases progressively from the periphery to
the cortex (Cajal, 1937). De Kock et al. (2007) have calcu-
estimate that a single whisker deflection generates about
4000 impulses in the cortex. This avalanche grows further
through the associated cortical areas, before it is funneled
down the final common path to the motoneuron, but even
with his great skills of preparation, observation, and imag-
ination, Cajal was unable to trace the route from input to
out reward, for he provided a comprehensive description
of the different cell types that inhabit the neocortex of dif-
ferent animals and incorporated the earlier descriptions of
cortical cell types of Retzius, Meynert, Betz, and others.
Lorente de No ´ (1949) pursued Cajal’s dream, also with
Golgi’s stain, and suggested that the functional unit of
cortex consisted of a specific thalamocortical fiber and
a cylindrical group of cells surrounding the fiber, some of
which formed synapses with the thalamocortical fiber.
With succeeding generations, however, this confidence
in a basic circuit became less secure, and there was even
a return, in the 1930s, to the idea that the neocortex was
an equipotential network (Lashley, 1930), an idea demol-
ished by Sperry (Sperry, 1947; Sperry et al., 1955), or
that the connections between cortical neurons were not
at all specific, but perhaps statistical (Sholl, 1956) or semi-
and Schu ¨z, 1991). Thus, proposals that the local circuit of
barrel cortex begins its life as a ‘‘tabula rasa’’ to be written
on by experience (Jeanmonod et al., 1981; Le Be and
Markram, 2006; Kalisman et al., 2005) are simply a contin-
uance of a surprisingly long-lived hypothesis that the
cortex really wants to be a randomly connected neural
In the face of such enormous numbers of possible cir-
cuits that could potentially arise from such random neural
networks, to pursue the concept that all of neocortex has
Figure 1. The Phantom Island of Buss
First ‘‘discovered’’ in 1578, it disappeared from the Nautical charts
after 1856. http://eaudrey.com/myth/Places/buss_island.htm.
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