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The Tripartite Synapse: An Elementary
Reflection Mechanism by Prof. Bernhard J. Mitterauer,
M.D. Institute of Forensic Neuropsychiatry and Gotthard Günther Archives Abstract
Initially a tripartite synapse is described which embodies a
synaptic model of glial-neuronal interaction. It consists of the presynaptic
and postsynaptic components, a synaptic cleft and the glial component
(astrocyte) which controls neurotransmission. Based on a biocybernetic model of
a tripartite synapse, the glial-neuronal interaction can be interpreted as an
elementary reflection mechanism. This reflection mechanism is essentially based
on the principles of two-places-mirroring, intention, feasibility, negative
feedback and rejection. Furthermore, it could embody standpoints of
self-observation in the synaptic microdomain. Although the cooperation of these
standpoints of self-observation in an undisturbed self-conscious brain seems
mysterious and difficult to research, the paper offers a new proposal as to how
and where elementary reflection mechanisms could be localized in the human brain.
Key words: tripartite synapse – glial-neuronal
interaction – biocybernetic model – reflection mechanism – standpoints of
self-observation 1. INTRODUCTION Presently, almost all brain oriented theories of consciousness are based solely on interpretations of the neuronal system of the brain, not referring to the glial system (for reviews see Black et al, 1998; Searle, 2004; Bennett & Hacker, 2004). In contrast to such exclusively neuronal approaches to consciousness, I have already proposed in several studies that the glial system in its interaction with the neuronal system could play a significant role in the processes underlying consciousness (Mitterauer, 1998, 2000b). Since glial-neuronal interactions have been experimentally well founded (Kettenmann & Ransom, 1995; Sykova et al, 1998; Haydon, 2001; Rouach et al, 2004), any comprehensive brain model or theory should take both systems of brain tissue into consideration. This paper focuses on glial-neuronal interactions in synapses, called tripartite synapses (Volterra et al, 2002; Auld & Robitaille, 2003). After the description of a tripartite synapse according to the model of Smit and coworkers (2001), a biocybernetic interpretation of this model as an elementary reflection mechanism is proposed. Supposing that tripartite synapses embody an elementary reflection mechanism, they could function as standpoints of self-observation. Since tripartite synapses of various transmitter types occur abundantly in the brain, it is a mystery how they cooperate in generating self-consciusness on the highest level of reflection. However, my proposal to localize elementary reflection mechanisms into tripartite synapses could be a first step towards a localization of consciousness processes in the synaptic microdomain of the brain. In considering the principles on which the reflection mechanism is based, this paper offers at least some new proposals for consciousness research in the neurosciences. 2. Tripartite Synapses According to the prevailing view, chemical synaptic transmission
exclusively involves bipartite synapses consisting of presynaptic and
popstsynaptic components and a synaptic cleft, in which a presynaptically
released neurotransmitter binds to cognate receptors in the postsynaptic cell.
However, there is a new wave of information suggesting that glia, especially
astrocytes, are intimately involved in the active control of neuronal activity
and synaptic transmission. Meanwhile, experimental
results are inspiring a major re-examination of the role of glia in the
regulation of neural integration in the central nervous system (Kettenmann &
Ransom, 1995; Bezzi & Volterra, 2001; Haydon, 2001; Auld & Robitaille,
2003). Glial cells (particularly astrocytes with their processes that contact
or even enfold a synapse) modulate the “efficacy of synaptic transmission”
(Mitterauer et al, 1996; Mitterauer, 1998, 2000a, 2000b, 2001a,
2001b; Oliet et al, 2001; Fields & Stevens-Graham, 2002; Mitterauer,
2003; Mitterauer & Kopp, 2003). Signals between astrocytes and neurons can
be mediated by glutamate (Gallo & Ghiani, 2001), acetylcholine (Smit et al,
2001), and other neurotransmitters (Kimelberg et al, 1998), but also by
intracellular calcium oscillations in astrocytes that have been hypothesized to
affect synaptic cleft calcium concentrations (Cooper, 1995; Newman & Zahs,
1997) and, subsequently, the amount of neurotransmitter released from
presynaptic terminals. In addition to modulating synaptic transmission in
neuronal cells, astrocytes may play a
direct role in generating pacemaker rhythms (Mitterauer et al, 2000; Parri et
al, 2001). More than a decade ago,
Teichberg (1991) suggested that glial kainate receptors play a role in
regulating synaptic efficacy and plasticity. Based on pertinent experimental
findings, she proposed a synaptic model composed of three mutually interacting
compartments: the presynaptic terminal, the postsynaptic membrane, and the
glia, the latter possibly carrying some of the machinery regulating synaptic
efficacy and plasticity. Until now, there is accumulating evidence that
synaptically associated astrocytes (and perisynaptic Schwann cells) should be
viewed as integral modulatory elements of tripartite synapses (Araque et al,
1999; Volterra et al, 2002). 3. Model of a Cholinergic Tripartite Synapse Smit and coworkers (2001) proposed a model of a cholinergic tripartite
synapse that might turn out to be a milestone for our understanding of the
glial-neuronal interaction. But first let me shortly describe this type of
tripartite synapse (Fig. 1). These authors identified a glia-derived soluble
acetylcholine-binding protein (AChBP), which is a naturally occurring analogue
of the ligand-binding domains of the nicotinic acetylcholine receptors
(nAChRs). Like the nAChRs, it assembles into a heptamer with ligand-binding
characteristics typical of a nicotinic receptor. Presynaptic releases of
acetylcholine induce the secretion of AChBP through the glial secretory
pathway, and once in the synaptic cleft, it acts as a molecular decoy, binding
the transmitter and reducing its availability at the synapse. This model, which focuses on
the role of AChBP in neurotransmission, suggests that there is a basal level of
AChBP in the synaptic cleft, maintained by continuous release from the synaptic
glial cells. Under conditions of active presynaptic transmitter release, high
millimolar concentrations of free ACh will probably activate both postsynaptic
receptors and nAChRs on the synaptic glial cells, which would enhance the
release of AChBP, thus increasing its concentration in the synaptic cleft. This
may either diminish or terminate the ongoing ACh response or raise the
concentration of basal AChBP to the extent that subsequent responses to ACh are
decreased. 4.
Biocybernetic Model of a Tripartite Synapse A simple biocybernetic model of a tripartite synapse could be helpful
for interpreting an elementary reflection mechanism. Generally, a living system
like man is endowed with intentional programs (hunger, desires, etc.) that
strive for realization in the environment (Iberall & McCulloch, 1969). This
intentional relationship of a living system with its environment can be
described as an elementary behavioral cycle (Mitterauer, 2000a). Information
from the environment actualizes an intentional program. If a living system is
able to find appropriate objects for realizing a specific intentional program
in the environment, then the cycle is closed, comparable to an experience. A
negative feedback mechanism breaks off the information processing (Fig. 2). Such elementary behavioral
cycles may also control the information processing in tripartite synapses. The
production of neurotransmitters in the presynapse can be interpreted as
“environmental information” stimulating the expression of BP in an astrocyte.
BP may embody an “intentional program” that is ready for occupancy by an
appropriate neurotransmitter. If an appropriate occupancy occurs (“realization
of an intentional program”), the glial system negatively feeds back this
“experience” to the presynapse. In parallel, this synaptic experience is
transmitted to other cells in the glial-neuronal networks by occupancy of
postsynaptic receptors (“information transmission”). Now, the cycle can start
again (Fig. 3). But what makes astrocytes so intentional?
In a series of papers, I have hypothesized that the glial system has a
spatio-temporal boundary-setting function in its interaction with the neuronal
system (Mitterauer et al, 1996; Mitterauer, 1998, 2000a, 2000b, 2001a, 2001b,
2003; Mitterauer & Kopp, 2003). With respect to a tripartite synapse, this
would mean that astrocytes control synaptic information processing by setting
temporal boundaries dependent on the occupancy of BP. In that case, glial BP
embodies an essential parameter of synaptic information processing. 5. Elementary Reflection Mechanism in
Tripartite Synapses Instead of attacking the difficult problem of consciousness or even
self-consciousness directly, my interpretation of a tripartite synapse is based
on the more basic concept of reflection. Formally speaking, reflection is an
act of recursion. In the basic case of recursion, the result of an act of
computation becomes the object (argument) of the same act of computation
(algorithm); thus switching between the outcome of an act and the object of the
same act. Therefore, recursion is nothing more than the formal description of
technical or biological processes based on feedback mechanisms. Feedback
mechanisms in biological brains are abundant and experimentally well
established (Damasio, 1992; Crick & Koch, 1995; Singer, 1995). If one
assumes that feedback mechanisms already carry out the principle of reflection
on this basic level, we must conform to Crick and Koch that feedback mechanisms
generating the synchronization of neurons in the cerebral cortex represent
elementary consciousness processes. These are not, however, self-conscious. But
what kind of role do feedback mechanisms play on the synaptic level, especially
in tripartite synapses? Could it be that the double structure of the brain in
the sense of both neuronal and glial cells represents the ontological
prerequisite for conscious processes? Let me start out with a
description of reflection based on a two-places-value system. According to Guenther
(1966), the method of reflection which the human or any brain necessary uses,
is a clear indication of the fact that the brain uses a place-value-system.
Because in order to be reflected a concept has to turn up in the brain at least
twice: once in the place where it originates and, second, in the place where
its “mirror image” is reflected. Without this capacity no brain is capable of
conscious awareness of anything. If we think of the world as a system of
reality and thought, we actually think the very concept twice: as bona fide
object and as reflection of the same. In order to keep both apart, the brain
has to “locate” the identical concept in two different “places” in its pattern
of awareness. My hypothesis is that Guenther’s conception of reflection can be
easily transferred to the biocybernetic model of a tripartite synapse as
proposed. According to my interpretation a tripartite synapse is constituted of the
following four principles: first, it consists of the neuronal and the glial
system and, thus, can be interpreted as a two-places-system. Second, the
neuronal synaptic system transmits information from other systems of the inner
and outer environment embodied by neurotransmitters. In parallel it activates
the glial system (astrocyte) via occupancy of the cognate glial receptors.
Third, the glial system determines the neuronal information processing by its
intentional programs embodied as glial binding proteins. Fourth, the glial
system is setting temporal boundaries by breaking off information processing in
the sense of a negative feedback. In other words: if the intentional programs
are realized or feasible, further environmental information is temporarily
rejected. Returning again to the method
of reflection according to Guenther (1966), a tripartite synapse embodies an
elementary reflection mechanism. Figure 4 shows a schematic diagram of that
mechanism. There are two “places”, i.e. place x embodying the neuronal system
and place y embodying the glial system. The basic concepts of the two places
are the following: the environmental information processing representing “bona
fide objects” occurs in the neuronal system. The glial system generates intentional
programs in the sense of “thoughts” activated from the neuronal information.
Since the concepts of the neuronal and glial systems are spatially separated, a
mirroring is possible, supposing that the “thoughts” correspond to the “bona
fide objects” in the environment. Such a synaptic architecture allows for an
active reflection of a mirror situation via a negative feedback mechanism. In
cybernetic terminology, feedback could embody purpose (Waldrop, 2001). Searle (2004) seems to be
right when he mentions that the problem of intentionality is something of a
mirror image of the problem of consciousness. According to the elementary
reflection mechanism proposed, intentionality may play a decisive role in
tripartite synapses, because a mirroring of concepts in a two-places-system
needs an active decision process based on an intentional program. Intentional
programs or thoughts are striving for realization (feasibility) in an
appropriate environment. This may occur within tripartite synapses via occupancy
of glial binding proteins with their cognate neurotransmitter embodying
appropriate environmental objects (“bona fide objects”), similar to perception
which is also action-oriented or intentional (Prinz, 1990), since a big amount
of information must be rejected in order to recognize intended objects,
subjects or situations. The same may occur in tripartite synapses. As soon as the
negative feedback mechanism works, the synaptic information transmission is
turned off, so that the environmental information is temporarily rejected. 6. Tripartite Synapses as
Standpoints of Self-Observation
Generally speaking, the prefix “Self” points out that a system is
capable of formal recursion or mechanic feedback. On higher levels as in the
human brain, terms like self-observation or even self-consciousness are based
on the ability of reflective thinking. Following my considerations so far, a
tripartite synapse can be interpreted as an elementary standpoint of
self-observation in the brain. I have already postulated that self-reflection
may be represented in a manifold manner in the brain (Mitterauer, 1998),
similar to the “Many Cartesian Theaters” (Damasio, 1992) or “many self-systems”
(Baars, 1996). Here I am attempting to describe a basic synaptic reflection
mechanism that could be underlying all higher level consciousness processes. One might argue that the
neuronal system is also compartmentalized per se (Rall, 1995; Mel &
Schiller, 2004). Furthermore, it is imaginable to see a many-place-system in
the neuronal compartments as such. But according to my view there is a
qualitative difference between the purely neuronal compartments and the glia
determined compartments (Mitterauer, 2003; Mitterauer & Kopp, 2003).
Neuronal compartments are merely functional for information processing, whereas
glial-neuronal compartments may in addition have an information structuring
potency based on the glial spatio-temporal boundary setting function
(Mitterauer, 1998, 2000b, 2003, 2004a). Taking the tripartite synapse as a
model system of glial-neuronal interaction in the sense of an elementary
reflection mechanism, the glial system (astrocyte) may contribute two basic
principles that could give rise to pure feedback mechanisms in the sense of
reflection mechanisms. One of these principles is intention, the other
rejection, as already described. Supposing that tripartite
synapses embody “micro-self-systems” which do not reach self-consciousness, we
are confronted with the mystery how self-consciousness arises in the brain.
This mystery is difficult to research. Current neuro-philosophical approaches
which exclusively concern the neuronal system try to localize self-systems in
various brain areas. From an anatomic-functional point of view, Baars (1996)
provides numerous examples (e.g. split-brain patients, sensorimotor homunculus)
which show that different self-systems can be represented in the brain. Damasio
(1994) refers to a “neuronal Self”. Edelman (1992) also states his opinion that
there is a biological self which he confines to subcortical homeostatic
systems. Although we know that certain areas of the brain have priority for
special tasks, it has not been possible to find a topological allocation for
the different and complex reflection processes or to localize self-systems. My proposal to localize
elementary reflection mechanisms into tripartite synapses could be a first step
towards a localization of consciousness producing processes in the synaptic
microdomain of the brain. But considering the different types of synapses that
codetermine our behavior via specific proteins (neurotransmitter, glial binding
proteins, etc.), and, in addition, the astronomic number (1014 to 1015)
of synapses in the brain, we are challenged with a combinatorial explosion in
computing possible interactions between the various types of tripartite
synapses. Most importantly, we have no formal definition of the concept of Self
available. An operational formulation could be: the Self is a living system
capable of self-observation (Mitterauer & Pritz, 1978). We should, however, be able
to find the part of the brain that integrates all of the different elmentary
reflection mechanisms or subsystems of the Self in the undisturbed
self-consciousness. Several decades ago, the group working with McCulloch
considered the reticular formation in the brain stem as an “integrative matrix”
(Scheibel & Scheibel, 1968) as well as a “central command system” (Kilmer,
McCulloch, & Blum, 1969). Lately, Newman (1997) has suggested an “extended
reticular-thalamic activating system” as a neural correlate for a “central conscious
system” (see also Steriade, 1996). According to Churchland (2002), the most
basic level of inner coordination and regulation occurs in the brain stem,
anchoring what Damasio (1999) refers to as “the protoself”. 7. Future Prospects
Admittedly, the
model of a tripartite synapse and its interpretation as an elementary
reflection mechanism is hypothetical. First of all, the glial binding proteins
must be identified in human brains. Presently we try to formalize a tripartite
synapse interpreted as an intentional multiagent system (Mitterauer &
Pfalzgraf, 2005). Such a robotic approach is promising, since the testing of my
model with neurophysiological methods might be impossible. Perhaps neuroimaging
could shed some light into the reflection mechanisms of tripartite synapses.
However, if we succeed to build such a model in a robot brain, then it could
teach us if we have a real biomimetic system.
In his book “the mind doesn’t work that
way”, Fodor (2000) speaks of “cognitive-neuro-science-fiction; there aren’t any
proposals”. Despite that harsh criticism, Fodor is right that there is
something like a stalemate in biologically based consciousness research. The
present paper represents a further modest attempt to refer to the whole brain
tissue in the sense of an interacting glia-neuronal double structure. To my
knowledge this is the first synaptic model which describes an elementary
reflection mechanism. It is based on principles like two-places-mirroring,
intention, feasibility, negative feedback and rejection. Is there perhaps one
or other proposal Fodor could be looking for?
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machine. Harmondsworth: Penguin Books. Figure 1. Model of the role of AChBP in
neurotransmission A basal level of AChBP is present in the synaptic cleft. Presynaptic ACh
release can lead to activation of postsynaptic receptors and to EPSPs. In
parallel, nAChRs on glia are activated, causing increased release of AChBP into
the synapse, which leads to suppression of cholinergic transmission (reproduced
from Nature, Vol. 411, May 2001, pp. 261-268, Fig. 8, with permission of first
author A.B. Smit and Nature Publishing Group). Figure 2. Elementary behavioral cycle An information from the environment activates one or more intentional
programs. If a living system is able to find appropriate objects for realizing
a specific intentional program in the environment, then the cycle is closed (—│),
comparable to an experience (Mitterauer, 2004a). Figure
3. Biocybernetic model of a tripartite
synapse The production of neurotransmitter (NT) in the presynapse provides the
system with “environmental information” stimulating the expression of glial
binding protein (glBP) in an astrocyte. GlBP may embody “intentional programs”
realized by appropriate neurotransmitter occupancy. If an appropriate occupancy
occurs, the glial system negatively feedbacks (—│) this “experience” to
the presynapse. In parallel, this synaptic experience is transmitted to other
systems by occupancy of postsynaptic receptors (Mitterauer, 2004a). Figure 4. Schematic diagram of an elementary reflection
mechanism in tripartite synapses. Place x (red) represents the neuronal component, place y (green) the glial
component of a tripartite synapse. After activation (arrow) of the glial system
by the neuronal system, the intentional programs (“thoughts”) are mirrored
(double arrow) to the environmental information (“bona fide objects”). A
negative feedback determines that the mirroring breaks off (fat bar) the
information processing (“embodiment of purpose”), which corresponds to an
elementary reflection mechanism.
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