The brain’s capacity rapidly to integrate information
from many different sources lies at the root of our cognitive
abilities. Two general questions are particularly relevant to
understanding this capacity. First, how is the specialized in-
formation conveyed by the activity of functionally segre-
gated areas and neuronal groups integrated into a unified,
coherent scene? This question underlies one of the oldest
controversies in neuroscience – that between localizationist
and holistic views of brain function. Second, how is the in-
formation that is conveyed by incoming stimuli integrated
with information present in memory? It is often assumed
that the brain controls behavior by processing incoming
stimuli in the form of neural activity patterns. On the other
hand, it is also assumed that the brain lays down memories
of previously encountered stimuli in the form of patterns of
connectivity among neurons. Consequently, information pro-
cessing and information storage are often studied separately
and with different methodologies.
In this review, we consider experimental evidence as
well as recent theoretical studies suggesting that the ques-
tion of how the brain integrates information can be ad-
dressed within a unified conceptual framework. We first
discuss known neural mechanisms underlying cognitive and
behavioral integration. We then examine a set of statistical
measures derived from information theory that can be used
to characterize the integration of information among func-
tionally segregated groups of neurons. Finally, after consid-
ering the key role of spontaneous activity in brain function,
we examine how these statistical measures can be used to
evaluate the integration of incoming stimuli with ongoing
neural interactions.
Functional segregation and integration
Phrenologists had imagined that different cognitive func-
tions were allocated to different parts of the brain well be-
fore any neurobiological evidence was available. Advances
in neuroscience appear to have fulfilled the phrenologists’
dream and have conclusively demonstrated that functional
specialization at multiple spatial scales is a fundamental
principle of brain organization. In the visual system, for ex-
ample, different brain areas are functionally specialized for
visual attributes such as shape, motion, and color
1–3
, and
parcellation of function has been discovered within other
sensory modalities and in the motor domain
4–6
. Functional
segregation extends to the level of columns or groups of
neurons
7
. In primary visual cortex neuronal groups are spe-
cialized for different stimulus orientations
8,9
, direction of
motion
10
and spatial frequency
11
. A similar specialization
along different stimulus dimensions has been discovered in
essentially every brain area that has been studied in suffi-
cient detail
12,13
. Most recently, it has been demonstrated
that different brain regions can be activated by specific cog-
nitive tasks or by specific stimulus attributes whether these
are perceived, imagined, or remembered
14
.
While the evidence for regional specialization in the
brain is overwhelming, it is clear that the information con-
veyed by the activity of specialized groups of neurons must be
functionally integrated in order to guide adaptive behavior
– just consider how many different signals must be rapidly
evaluated and coherently integrated to navigate safely in a
busy city. Like functional specialization, functional in-
tegration occurs at multiple spatial and temporal scales. In
vision, for example, individual elements (dots, edges) are
474
Complexity and
coherency: integrating
information in the
brain
Giulio Tononi, Gerald M. Edelman and Olaf Sporns
The brains of higher mammals are extraordinary integrative devices. Signals from large
numbers of functionally specialized groups of neurons distributed over many brain
regions are integrated to generate a coherent, multimodal scene. Signals from the
environment are integrated with ongoing, patterned neural activity that provides them
with a meaningful context. We review recent advances in neurophysiology and
neuroimaging that are beginning to reveal the neural mechanisms of integration.
In addition, we discuss concepts and measures derived from information theory that
lend a theoretical basis to the notion of complexity as integration of information and
suggest new experimental tests of these concepts.
G. Tononi, G.M.
Edelman and
O. Sporns are at
The Neurosciences
Institute, 10640 John
J. Hopkins Drive,
San Diego,
CA 92121, USA.
tel: +1 619 626 2000
fax: +1 619 626 2099
e-mail: tononi@nsi.
edu
Review Tononi et al. – Complexity and coherency
1364-6613/98/$ – see front matter © 1998 Elsevier Science. All rights reserved. PII: S1364-6613(98)01259-5
Trends in Cognitive Sciences – Vol. 2, No. 12, December 1998