December 12, 2002 8:51 WSPC/179-JIN 00008

Journal of Integrative Neuroscience, Vol. 1, No. 2 (2002) 145–156

c Imperial College Press

Short Communication

TOWARDS AN INTEGRATIVE THEORY OF COGNITION

ROMAN R. POZNANSKI
Centre de Recherche en Physiologie Intégrative, Hôpital Tarnier,
CHU Cochin-Port-Royal, 89, rue d’Assas, Paris 75006, France
poznan@integrative-physiology.org

Received 6 March 2002

Accepted 18 August 2002

A framework is outlined for connecting brain imaging activity with the underlying bio-
physical properties of neural networks, and their mechanisms of action and organizing
principles. The main thrust of the framework is a dynamic theory of semantics based on
functional integration of biophysical neural networks. It asserts that higher-brain function
arises from both synaptic and extrasynaptic integration in the neuropil where information
on environmental changes is represented dynamically through a discourse of semantics.
Consequently, integrative neural modeling is shown to be an important methodology for
analyzing the response activities of functional imaging studies in elucidating the relation-
ship between brain structure, function and behavior.

Keywords: Local field potentials; biophysical neural networks; functional connectivity;

neuropil; multi-hierarchical modeling; fMRI.

1. Introduction
The cerebral cortex works by activating distinct multiple neuronal populations, each
cortical population having connections (e.g., associative, commissural, and projec-
tion fibers) to other large-scale neuronal populations (see [13, 36]). This makes it
difficult to evaluate the functional contributions of a single large cortical popula-
tion with electrophysiological techniques, such as with multi-unit microelectrodes.
Brain imaging devices have a spatial resolution that is large compared with the
size of neurons. A single voxel may reflect 30,000 or more neurons activated simul-
taneously, and therefore multiple neuronal populations are easily investigated in
any resolvable region of interest. However, such a spatial resolution involves a high
degree of interconnectedness at the neural systems level. To explore the essence
of these interactions, and therefore create realistic large-scale theories of cortical
neuronal circuitry is a major challenge (e.g., [20, 45]). Indeed, the essence of such
interactions requires integrating multi-disciplinary data from protein sequences to
behavior into realistic models. This is one of the greatest challenges to contemporary

145
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146 Poznanski

neuroscience [41], and which requires exploration through the notion of integration
in the brain [25].
The application of various imaging devices to investigate brain function is an
important goal of integrative neuroscience. Functional neuroimaging studies can
provide information about the neuroanatomical and functional organization of the
brain by mapping brain activation associated with a variety of cognitive processes
(e.g., [19, 37]), but studying changes in the activity of specific regions of the brain to
reveal the organization of neural networks involved in cognition requires a theoretical
understanding through the development of mathematical models (see [24] for an
overview). Recent work dealing with so-called “structural equation modeling” [46]
to bridge the gap between imaging and the underlying neural networks of the brain
provides some impetus in this direction. However, integrative neural modelsa of the
cerebral cortical circuitry are probably the only way to arrive at predictions that can
be tested experimentally. This is because brain regions may be indirectly connected
to other brain regions, and therefore functional connectivityb between brain regions
must be evaluated, that is indicative of the interregional connectivity, and not just
how correlated their activities seem to appear.
Synchrony is a good indicator of neural correlation activity. A pre-condition for
correlation activity is induced oscillatory fluctuations of the membrane potential
associated with periodic activation of voltage-gated (sodium) conductance in den-
drites as a result of sinusoidal or cyclic current input, and in some species aided by
widespread gap-junctional coupling among specific types of neurons. Correlation ac-
tivity can therefore be evoked for example, by the application of a cyclic (sinusoidal)
current input to biophysical neural networks that are electrotonically coupled. Syn-
chronized neural activity enshrines the notion of brain activity being dynamically
coherent, but not necessarily integrative. For example, the binding operation such
as synchronized firing of neural assemblies in concert is epiphenomenal and not an
integrative mechanism of brain function. This is because when two spatially distinct
neuronal systems are activated synchronously (temporal) in response to a stimulus,
this is not an indication that the neuronal systems are functionally connected, but
simply are dynamically coherent. To dynamically associate selected subsets of active
neurons into functionally coherent assemblies based on synchronization of neuronal
responses is what is referred to as neuronal transients [18].
It is possible to measure the activity of neuronal transients with modern brain
imaging methods to reveal spatio-temporal features of complex behavior (e.g., [15]).
Many brain imaging experiments with functional magnetic resonance imaging
(fMRI), positron emission tomography (PET) and magnetoencepalography (MEG)
are required to characterize the contribution of each cortical population and the ef-

a Integrativeneural modeling is a precursor to synthetic neural modeling — a multi-hierarchical theoretical

approach to the problem of understanding the neuronal bases of adaptive behavior (see [38]).
b Functional connectivity refers to neuronal pathways (not necessarily connected anatomically) that emerge

from spatio-temporal activity patterns in response to specific cues.

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Towards an Integrative Theory of Cognition 147

fective connectivity c between these cortical populations [17]. The microstructure of

the cerebral cortex, thalamic nuclei, basal ganglia and other sub-cortical structures
in the brain is not apparent by brain imaging to evaluate the effective connectivity of
the neural networks. These methodologies do not possess the temporal resolution to
investigate transient changes in the relationship between cortical populations during
cognitive processing. Furthermore, neuroimaging cannot provide clear evidence that
neurons, neural circuits and brain regions have functionally meaningful complex
nonlinear neural dynamics. Moreover, neuroimaging cannot reveal how information
is represented in the brain. Therefore, it is clear that integrative neural modeling is
complementary to brain imaging in the investigation of dynamic cortical integration
of brain activity.
The key question this short communication will aim to address, is how the dy-
namic changes to functional connectivity can be differentiated from the neuronal
transients observed using neuroimaging technologies. It will be shown that neu-
roimaging response characteristics across various spatial and temporal scales need to
be juxtaposed with both the dynamics of biophysical neural networks and dynamic
phenomena such as volume transmission for a greater understanding of integrative
brain functions [21].

2. Syntactical Representation of Functional Connectivity

The diverse activities of numerous neurons in the brain coalesce through the dy-
namic coupling of neuronal groups [9]. These dynamically generated assemblies of
neurons lead to the formation of topographic maps showing the spatial distribu-
tion of responses in the brain [14, 35, 48]. Syntactical representations of functional
connectivity emerge from topographic maps (or global mappings) encompassing the
integration of thalamocortical pathways [10]. The stress is on integration as pre-
viously defined topographic maps, such as the Kohonen maps [27] do not exhibit
realistic structural characteristics needed for neuronal integration.
How is functional connectivity differentiated from the myriad of synaptic con-
nections between neurons in networks? A highly dynamic environment serves as a
catalyst for the emergence of functional connectivity from synaptic connectivity.
The mechanism of emergence is not holistic (i.e., Gestalt), but depends on dy-
namic changes to functional connectivity through adaptive pressures referred to as
“functional productivity” [22]. This pressure alters functional connectivity through
neuromodulation, a process through which this occurs is nonsynaptic diffusion neu-
rotransmission [3]. Thus, post-ontogenic functional organization is malleable under
adaptive pressure driven by diffusion and may be considered as a complex dynamical
system.
Consider for example, a neural system as a dynamical system, and apply topologi-

c Effectiveconnectivity refers to pathways directly connected anatomically that emerge from spatio-temporal
activity patterns in response to specific cues.
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148 Poznanski

cal arguments to illustrate the type of dynamic interactions involved. Any dynamical
system can be described by a number of variables. An abstract space, constructed
from the possible values of these variables, is called the state-space. The dynamic
evolution of a system can be described as a set of trajectories within its state-space,
and adjacent trajectories converge to form regions called hypervolumes in the state-
space. If all trajectories converge on a particular hypervolume it is called the basin
of attraction of that hypervolume. The direction of trajectories determines whether
or not the hypervolumes are attractors, repellors or saddle-points. Attractors are
regions in multi-dimensional space where the trajectories of the system coalesce and
fall into three types of behavior: point attractors, limit-cycle attractors and strange
attractors. For point attractors, the trajectories of the system converge to a single
point in the hypervolume, while for limit cycle attractors, the trajectories of the
system converge on a loop. Strange attractors are highly dependent on the initial
conditions and their trajectories tend to converge chaotically. Although such dy-
namical systems are explored in computational models (e.g., [12, 23]), they reflect
a nonspatial dependence, and therefore are incapable of fully describing brain dy-
namicism in terms of topographic maps of syntactical representation of functional
connectivity.
In order for dynamical systems to be reflective of the emergence of functional
connectivity, it is essential to include spatial dependence, so that these hypervolumes
are representations of spatio-temporal activity within the brain. The procedure re-
quires compatibility between bifurcations of high-dimensional problems with those in
low-dimensional spaces (Rn ). Infinite-dimensional problems in Banach space (Rn+1 )
fit the description of functional connectivity to be defined through spatio-temporal
activity patterns interpreted within the framework of brain dynamicism described
below, yet projection of the problems into low-dimensional space (like those with
discrete space) do not guarantee identical bifurcations. The Fredholm alternative
(e.g., [28]) for the solvability of the equations arising in the construction of the bi-
furcating solution may not hold under such projections, although the computation
of bifurcations does not require it to hold, and therefore computational approaches
investigating nonlinear dynamical systems with discrete space remain controversial
in their faithfulness in reproducing accurately the dynamics leading to a syntactical
representation of functional connectivity (see also [16]).

3. A Biophysical Basis of Brain Dynamicism

Neural networks represent a critical chasm in theoretical neuroscience- a level at
which cognitive operations connect with cell biology [31]. Yet, traditional connec-
tionism is firmly grounded in a Cartesian concept of mind as having no spatial
dimensions. To avoid Cartesian mind-body dualism, cognitive processes emerging
from brain imaging activity must be firmly grounded in the biophysical properties
of synapses and neurons located in three-dimensional space. As well, cognitive pro-
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Towards an Integrative Theory of Cognition 149

cesses have been shown to be distributed among specialized brain regions yet inte-
grated through specific connections. If specific connections at the mesoscopic level
arise from random organization at the cellular level, then functional connectivity is
synergetic rather than integrative. This is because integration requires a precisely
ordered topological mapping at each hierarchical level of neural organization. The
notion of local segregation (or differentiation) with global interaction (or integra-
tion) has similar connotations to the “randomness in the small, and structure in
the large” principle advocated by Anninos et al. [1]. The paradox can be resolved
if there is continuity among the repertoire of possibilities, so that the functional
operations converge to a dynamic core [47].
Cognitive abilities are intimately linked to the morphology of individual neurons
[11], yet are not localized within any group of specialized cells. Implicit inclusion
of biophysical properties, as well as the number of synapses of each neuron in the
network would enable local encoding or “grandmother cell” theories [4, 5] to capture
brain dynamicism during cognitive tasks without converging onto a fixed anatom-
ically defined sets of “grandmother cells”. By way of example, consider m = total
number of cortical neurons, n = total number of synaptic connections per neuron,
and p = total number of dendritic clusters of various ionic channels and G-proteins
lumped together as “hot-spots” including all types of neural transmitters, different
enzymes and other molecular substances, all regulating the neuromodulatory envi-
ronment per neuron. If m = 1010 and n = 103 [7] then the total number of unique
possibilities for local encoding in the cortexd (conceptualized on the assumption that
neural assemblies are structurally undistributed representations of real neural net-
works) is about 1013 . Whereas a human brain with inclusion of distributed neuronal
systems and their biophysical properties (e.g., p > 107 ), allows the total number of
possibilities for local encoding to be infinite. It should be mentioned that in nonhu-
man species both m, n, and p are significantly lower. For example, n = 800 in mice
and 20,000 in monkeys, but 40,000 in humans; m = 106 in rats, 109 in macaques and
1011 in humans [39]. It is bewildering to speculate on the species difference for p.
The significance of a greater p will have a direct bearing on integrative mechanisms.
Therefore, a human brain containing 10 billion cortical neurons, with about 10 tril-
lion possibilities for local encoding (i.e., p = 0) will not be sufficient to allow for
an infinite number of possibilities to be associated with a particular quale which is
unique for each functional connectivity of the biophysical neural network. However,
inclusion of biophysical properties in distributed neuronal systems (i.e., p 6= 0)
yields an infinite number of possibilities for local encoding needed to overcome the
combinatorial explosion associated with an infinite number of different possibilities
of qualia, and thereby circumventing the “binding” problem [34].
Local encoding on patches of dendrite is difficult to measure electrophysiolog-

d Assume p hot-spots are distributed spatially along the somatodendritic axis of each cortical neuron, with
p! possible unique combinations for local encoding. Also assume a simple feedforward cortical network, with
each synaptic connection corresponding to a possible unique local encoding. Therefore the total number of
unique possibilities for local encoding in the cortex is n(m − 1)p!.
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150 Poznanski

ically, but possible through integrative neural modeling (see next section). Dis-
tributed encoding of a neuron provides the representation through the requirement
that the biophysical properties of dendrites, superimposed at spatially distributed
locations, each contribute with different responsiveness through alternations in func-
tional connectivity. As a result, distributed encoding does not suffer from the combi-
natorial explosion problem (i.e., fresh neurons are required for every new object that
has to be represented) as this would be reflected in changes to local encoding on the
dendrites. Also objects or events do not fire infrequently because the “grandmother
cell” that provides the representation is integrated within a group or ensemble of
cells, each having a somewhat different responsiveness from the “grandmother cell”.
Rolls and Treves [39] reject the “grandmother cell” concept on grounds that no
such cells exist (i.e., in all cases the same neuron fires spikes to different stimuli).
However, it does not rule out local encoding because if information is represented
in the dendritic neuropil then the firing rate of individual neurons will only have an
indirect bearing on cognitive function, contentiously perceived to be coded in the
neural spike train.

4. Elucidating Interregional Connectivity Through

Integrative Modeling
It has been known that cerebral blood flow is closely coupled to neuronal metabolism,
which in turn is closely coupled to neuronal activity as observed under imaging. Yet,
the relationship between functional brain imaging and neuronal activity has only
been defined implicitly. Recent experimental studies correlating the spatial patterns
of haemodynamic responses associated with fMRI signals with changes to neural
activity in a form of local field potentials [30], gives strong impetus for modeling
biophysical neural networks in a neuropil to refine and quantify imaging of brain
function. For example, fMRI reflects the extrasynaptic activity of neurons [30], yet it
is unknown if both excitatory and inhibitory synapses produce similar fMRI signals,
so integrative neural modeling can help to predict the effects of various types of neu-
rotransmitter released, as well as reveal how the sequence and distribution of various
proteins (such as ionic channels, gap-junctions, and G-proteins), offsets the collec-
tive behavior of large masses of neurons in the neuropil, as reflected in neuroimaging
studies. Therefore, integrative neural models can provide a clear framework to in-
vestigate how synaptic activity in the neuropil is reflected in brain imaging activity.
In earlier work, local field potentials were simulated using continuum models
of neural networks. The approach entailed modeling large assemblies of neurons as
lumped nodes in a one-dimensional neural sheet or layer, rather than as popula-
tions of discrete networks. A field description for the neuronal density and local
field potential was determined for the spread of firing activity between neural as-
semblies via pseudo connections and delays without taking into consideration the
spatial distribution of neural masses. The extension of the continuum models to spa-
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Towards an Integrative Theory of Cognition 151

tially distributed neural aggregates, began with the so-called “current source density
analysis”. Here a microscopically inhomogeneous neural tissue was replaced with a
macroscopically homogeneous medium where electrical properties are represented
as averaged quantities in a volume of tissue representing the dendritic activity of a
group of neurons. This results in a simple relation between the local field potential
and the current source density of an averaged neural mass of neurons. Unfortu-
nately, it does not take into consideration the individuality of each neuron in the
neuropil. A more integrative approach that allows for the consideration of trans-
membrane current density of an individual neuron in a volume conductor and its
relationship with local field potentials requires each neuron to be represented as a
core-conductor (i.e., a cable with extracellular sheath surrounding the core) at the
microscopic level, while at the macroscopic level, as nodes, in a three-dimensional
realistic, inhomogeneous volume conductor. In particular, volume conductor model-
ing of local field potentials at the macroscopic level can be interpreted in terms of
cellular activity (e.g., extrasynaptic signals) at the single neuron or molecular level
by a Nernst–Planck analysis for the concentration of each ion in the neuropil. Such
multi-hierarchical modeling capture the essence of intra-cortical pathways exhibited
throughout the neocortex (i.e., cerebral cortex).
Determining interregional connectivity requires dynamic changes to functional
connectivity (resulting from recurrent interconnections within a neural network
and/or through volume transmission where the signal diffuses into a local volume
or neuropil) to be conceptualized in prototype models through imbedding of the
biophysical neural network in a volume conductor that interacts with the external
micro-environment. Indeed, MacLennan [32] has stressed the importance of develop-
ing a mathematically tractable and biologically plausible model of the neuropil that
includes closely packed matrix of dendrites, axons, somas and glia as precursor con-
ditions for complex interactions to take place in a system of ion fluxes, extrasynaptic
potentials and neuromodulators of neuronal activity. In particular, cortico-cortical
connections require a geometrical organization with both local and global coordi-
nates, in order to faithfully connect integrative neural modeling with functional
brain imaging studies. A high degree of interconnectedness at the neural systems
level requires models to explore the essence of these interactions (e.g., [43, 44]). The
integration of neural systems requires the utilization of n-field theory of biological
neural networks [6].

5. Dispositional States of Dynamic Representations of

Functional Operations
Topographic maps are not fixed neuronal assemblies or fixed patterns of activity, but
are specifically connected functional groups of neurons of distinct multiple neuronal
populations defined on the basis of a particular neurotransmitter (e.g., cholinergic,
serotonergic, dopaminergic and noradrenergic pathways). Such pathways serve as a
substrate for the functional integration of various neuronal systems correlated with
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152 Poznanski

ambient environmental variables through adaptive pressures referred to as dynamic

representation of functional operations [29].e
How does meaning or semantics follow from a particular dynamic representation
of functional operations? If the meanings are not intrinsically imbedded, but reflect
a dispositional state that has no syntactical representation [8] then how do existing
dynamic representations of functional operations remain intact? Dispositional states
require a subtle change to occur at the synaptic junctions, possibly involving the
extracellular matrix surrounding the synaptic boutons through nonsynaptic diffu-
sion via volume transmission. Indeed, neuroglia complete a tripartite configuration
in which they can modulate signals through synthesis and release of neural trans-
mitters [2]. One example of a mechanism for strengthening synaptic connections
without effecting the long-term changes in the neuronal synaptic elements is gluta-
mate activating AMPA-type receptors in neuroglia. The outcome is a rapid influx
of intracellular Ca+2 resulting in a retrograde Ca+2 release of glutamate from neu-
roglia, followed by activation of NMDA-type receptors on the presynaptic neuron,
increasing the release of glutamate and enhancing synaptic transmission. Recent
studies suggest that much of the metabolic activity, that is measured in neuroimag-
ing studies, can be attributed to neuroglia, which mediate metabolic demands of the
transmitter re-uptake process at glutamatergic synapses throughout the cortex [33].
Semantics, through an enormous variety of discourses in the synaptic pathways,
provide a substrate for observer-dependent meaning from outside the neural system
[40]. In other words, meaning is observer-dependent, and so the dynamic discourses
of the neural networks capture the semantics through a self-referential mapping of
specifically connected functional groups of neurons. Cognitive preceptsf emerge from
specifically connected functional groups of neurons in the temporo-parietal cortex
[26] through a self-referential mapping of dispositional states of dynamic represen-
tations of functional operations and semantic interpretation. The neurobiology of
semantics requires a priori integration of dynamic representations of functional op-
erations for each particular cognitive precept to be semantically interpretable. The
integration of dynamic representations of functional operations is dependent on the
notion of continuity and differentiability among a repertoire of possibilities. The
problem is to determine how information represented in the neuropil converges to
provide an appropriate internal representation in the context of embodied cognition
[42]. The approach requires anatomical association of the brain with a self-referential
mapping between dispositional states of dynamic representations of functional oper-
ations and a discourse of semantics, interpretable through environmental changes. A
semantic relationship between the intrinsic properties of the brain and the external
state of affairs in the environment remains unresolved and therefore a framework,

e Dynamic representations of functional operations are topographic maps of the dynamic changes to func-
tional connectivity.
f Cognitive precepts (e.g., perception, planning, attention, altruism, intuition and reasoning etc.) or higher-

brain functions involve a self-referential mapping between dispositional states of dynamic representations
and a discourse of semantics interpretable through environmental changes.
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Towards an Integrative Theory of Cognition 153

for further research to be carried out in the future. We envisage that an explicit cor-
relation between various cognitive precepts emerging from environmental changes
to be noncomputational.

6. Summary
In this paper, a novel theoretical framework of embodied cognition was presented,
allowing for the existence and use of internal representations, whereby informa-
tion is represented in the neuropil as a result of a collective effort attributable to:
(i) dendritic integration (including synaptic integration); (ii) extrasynaptic diffusion
of ions; (iii) glia for imbedding. Through adaptive pressures, the micro-environment
is highly malleable so therefore there are no fixed templates. These changes invoke
regions for high concentrations of ionic diffusion to be imbedded, aided by a network
of glia that temporarily stores the information. The increased capacity for cognitive
precepts to emerge from such changes was shown to be dependent on the syntactical
evolution of functional connectivity driven by adaptive pressures. In other words,
the functional organization of the brain increases the representational capacity to
account for high-level cognitive phenomena by allowing cognitive precepts to be
catalyzed through the biophysical structure of each neuron in the neuropil.
It may be said that consciousness or self-awareness is the final product of inte-
gration in the brain [25]; and not specifically through the thalamocortical pathways
that sustain distributed activity patterns [47]. The crucial step in the biophysics
of cognition is semantics. Semantic interpretation of the environment (e.g., social,
cultural, moral etc.) is defined through specific dynamic representations of func-
tional operations. If topographical maps of the parietotemporal cortex (i.e., area
that lies around the boundary between the parietal association cortex and the tem-
poral association cortex) trigger specific cognitive attributes, through an aggregate
of disparate yet continuous dynamic representations of functional operations, then
the neural basis of cognition becomes more viable for theoretical exploration and
subsequent vindication.

Acknowledgment
I thank Professor K. N. Leibovic for helpful comments on the manuscript.

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