SINGLE-NEURON THEORY OF CONSCIOUSNESS
Steven Sevush
Departments of Psychiatry and
Neurology
University of Miami School of
Medicine
1400 NW 10 Ave, Suite 702
Miami, Florida 33136
ssevush@med.miami.edu
Tel: 305-243-4082
This work was presented in abstract
form at
"Toward a Science of
Consciousness" held in Tucson, April 2002.
ABSTRACT:
A theory
is outlined that shifts the presumed locus of mind/brain interaction from the
whole brain level to that of single neurons.
Neuroanatomical and neurophysiological evidence is offered in support of
the existence of single neurons that may individually receive dendritic input
of sufficient complexity and diversity to account for the full content of
conscious experience, and of an arrangement in which the output of multiple
such neurons summate to achieve amplification of the individually emitted
messages. An ultramicroscopic extension
of the theory is suggested as a way of moving forward on the philosophically
difficult aspects of the mind/brain problem.
1.
INTRODUCTION
The
purpose of this paper is to suggest a shift in emphasis from the large to the
small in the search for a brain correlate for the mind. By most accounts, the mind is assumed to
correlate with the integrated activity of large populations of neurons
distributed across multiple cortical and subcortical brain regions (Sperry
1969, Damasio 1999, Edelman and Tononi 2000, John 2001). Nonlinear dynamic mechanisms are then
invoked to provide for the "binding" of the dispersed neuronal
activity into a unified stream of consciousness (Hardcastle 1994). By this view, activity within any single
neuron correlates with merely a fragment of the total conscious experience; it
is only through the integration of these fragments that a single whole-brain
consciousness is assumed to emerge.
A
contrasting model is outlined in the present paper that places the mind/brain
interface not at the whole brain level but at the level of the single
neuron. Specifically, the model
proposes that a single brain at any given moment harbors many separate
conscious minds, each one assumed to be associated with the activity of a
different individual neuron. The model
proposes, that is, that what is usually regarded as a person’s single conscious
experience correlates not with an integrated neuronal network, but individually
with single neurons that separately and redundantly encode the entire conscious
content. Consequently, at any given
time, a multitude of conscious beings are assumed to be associated with a
single person’s brain, all having identical or at least similar
experiences. Axonal outputs from
multiple such neurons are then conjectured to summate, providing amplification
of the message being emitted by any one of them. The overall scheme is one in which conscious behavior, while
appearing to be the product of a single macroscopic mind, is actually the
result of the superposed output of a chorus of minds, each associated with a
different individual neuron.
The
proposed theory makes the following assumptions:
a) Each
neuron in the nervous system is independently conscious, the electrical
activity in each neuron's dendritic tree serving as the neural correlate of
consciousness (NCC) for that neuron.
b) For
most neurons, such as those in the hypothalamus or those in the posterior
sensory cortices, or for cortical interneurons, the conscious activity of the
neuron would be expected to be simple and would additionally be unable to
directly affect the organism's macroscopic behavior. Such neurons would not, therefore, contribute to what is usually
taken as a person’s conscious behavior.
c) For a
subpopulation of neurons in the lateral prefrontal cortices, however, the
arrangement is such that: i) the
conscious activities of the individual neurons are of a complexity and diversity
sufficient to match that usually ascribed to the much of the brain as a whole;
and ii) a large number of such neurons having more or less the same conscious
activity at any given time summate their outputs to achieve amplification of
the message emitted by any one of them.
d) As a
result of this arrangement, the conscious content of an organism's macroscopic
behavior is seen to derive from the summated action of an ensemble of
independently conscious neurons.
Consequently, single neurons in the model serve independently as
separate NCC's; there is no combining of the individual consciousnesses into a
superordinate whole-brain consciousness.
The most
immediate implication of this arrangement is that it offers a novel approach to
solving the "binding problem," the problem of explaining how
spatially dispersed neuronal activity can correlate with an apparently seamless
single experience. The currently
popular view is that the NCC consists of a widely dispersed network of
electrically interacting neurons.
Proponents of this view commonly argue either that: a) perceptual unity
is achieved through temporal synchrony of the component elements (eg, via 40 Hz
gamma frequency oscillations), or b) perceptual unity is an illusion, as argued
by Dennett (1991). These approaches
have their difficulties, however (Revonsuo 1999, Chalmers 1996). The theory presented in this paper proposes
an alternative explanation for perceptual binding. The argument is that the entire content of conscious experience
correlates with activity at the level of the individual neuron, with perceptual
unity being achieved by spatial convergence of incoming signals upon such
neurons.
Of course,
there is then the question of how perceptual binding at the microscopic level
of the individual neuron is supposed to occur.
After all, neurons themselves have many subcellular components, so a
theory that shifts the NCC from the macroscopic network level to the
microscopic neuronal level only changes the locus at which perceptual binding
is assumed to occur. It does not by
itself explain how this binding is to be accomplished. Accordingly, at the end of the paper, in a
section entitled “Speculative Implications,” I outline a scheme by which
perceptual binding at the microscopic neuronal level might in fact be
explained.
With
regard to terminology, when the terms "mind" and
"consciousness" appear in this paper, they are being used in the
specific sense that Chalmers uses the term "experience" in his
discussion of the easy and hard problems of consciousness (Chalmers 1996). As described by Chalmers, the
"easy" problems of consciousness are those that appear tractable by
the usual methods of science and include the ways in which the brain focuses
attention, integrates information, controls behavior, and so on. In contrast, the "hard" problem of
consciousness is the problem of accounting for the content of subjective
experience, that elusive datum that appears to accompany certain high level brain
processes. Why does the electrical
processing in the brain that ensues when one looks at the sky give rise to the
experience of "blue" and not to the experience of some other color,
or to no color experience at all? In
what follows, it will be to consciousness in this sense that a neural correlate
will be sought.
The
legitimacy of employing "experience" as a target of scientific
investigation is not, it should be noted, universally accepted. It has, for example, been argued by Dennett
(1991) and others that "experience" is an illusion and that once all
the brain processes associated with a given behavior are objectively described
there is nothing left to be explained.
Dennett's arguments, if correct, would eliminate the need to localize a
mind/brain interface or to solve a "binding problem." If, on the other hand, subjective
experience is a phenomenon in need of explanation, then the proposed
single-neuron theory, which shifts the locus of the mind/brain interface from a
macroscopic to a microscopic domain, might provide fresh avenues for addressing
Chalmers' "hard problem."
Again, in the section of the paper entitled “Speculative Implications” I
will provide a specific example of how this might play out.
In what
follows I will outline the single-neuron model and argue for its feasibility
given what we know of brain architecture, noting in particular that a) the
dendritic trees of single neurons appear to provide for encoding of sufficient
complexity to account for the complexity of conscious experience, and b) that a
simple method of summing neuronal outputs may be available that could explain
the illusion of a single macroscopic consciousness. I will then discuss the empirical predictions made by the model,
the presence of which renders the theory falsifiable and therefore of a
scientific nature. I will then conclude
by offering a brief speculation as to how the model might be extended to a yet
more microscopic domain, and how this extension might be used to formulate a
framework for addressing the philosophically difficult aspects of the mind/brain
problem.
The model,
it should be stressed, is at this point presented as a hypothesis, not a proven
theory. The contention, given the data
presently available, is not that the proposed single-neuron mechanism is
necessarily the way the brain processes information, only that it is a possible
way for it to accomplish the task and that it should not be dismissed out of
hand. As will be seen, the model does
make testable predictions that will allow for eventual adjudication of its
validity. There is no question that the
theory takes a stance that is at odds with prevailing intuitions. Yet, the stakes are high and, in view of the
difficulties inherent in the mind/brain problem, unusual approaches to its
solution may be warranted.
2.
THE POSSIBILITY OF MULTIPLE TYPES OF CONSCIOUSNESS
Before
proceeding to an explication of the theory, it is necessary first to deal with
a potential ambiguity that may arise from the assumption that multiple minds
are present in a single brain. As will
be seen, this assumption will play centrally in the theory to be presented in
this paper, both at the macroscopic and the microscopic levels. The problem is that if there are multiple
consciousnesses present in a single brain, then it becomes possible that
consciousnesses of different types might be included in the set. Consequently, a potential ambiguity may
arise with regard to the meaning of the term "consciousness." That is, when the term is used, to which of
the different kinds of consciousness would it be meant to refer?
In order
to minimize the potential for ambiguity of this kind, the theory will initially
be presented for the restricted case of verbally reportable consciousness
(designated in this paper as "VR-consciousness"), by which I mean
consciousness that has direct access to verbal report. The restriction is not intended to imply
that VR-consciousness is the only type of consciousness present nor that
VR-consciousness is necessarily imbued with any special properties. Nor is it implied that verbal output is the
only form of behavior that can be influenced by VR-consciousness. The restriction is introduced only
temporarily and as a convenience to minimize ambiguity in the initial
presentation of the theory.
VR-consciousness has been chosen for this purpose because it is around
this form of consciousness that the debate over the hard problem of
consciousness has been primarily focused.
Once the theory has been examined for the special case of
VR-consciousness, the argument will then be expanded to address the potential
existence of other types of consciousness.
Armed with
these preliminaries, we can now turn to the presentation of the model. A sketch of the single-neuron theory for
VR-consciousness will be developed in two steps, one macroscopic, the other microscopic. In the macroscopic step, the suggestion will
be made that much of the distributed brain processing often considered to
correlate with VR-consciousness may in fact be only preliminary to VR-conscious
experience, and that only when the processed information is accessed by a
particular focal area, namely the left[1]
lateral prefrontal cortex (PFC), does it achieve VR-conscious status. In the microscopic step, it will be argued
that VR-consciousness is mediated not by the left lateral PFC as a whole, but
separately and redundantly by individual pyramidal neurons inhabiting the
region. On the input side, a model of
redundant convergence upon individual neurons within the population will be
offered and support for its plausibility presented. On the output side, a mechanism will be described by which the
signals emitted by the VR-conscious neurons might be summated, yielding the
illusion that a single macroscopic VR-consciousness is present. Finally, the theory will be extended to
account for consciousness of a non-verbally reportable variety.
3. THE MACROSCOPIC STEP: PLAUSIBILITY OF A FOCAL MODEL
The first
objective in developing the single-neuron theory is to determine, on a macroscopic
level, just which brain region or regions participate directly in VR-conscious
experience. The commonly held view is
that it is the activity of neuronal populations dispersed across multiple
cortical and subcortical brain regions that mediates VR-consciousness (Damasio
1999, Edelman and Tononi 2000, and John 2001).
On the face of it, this multifocal view seems mandatory. It is indeed difficult to imagine how, instead,
a single brain region could manage to receive a repertoire of inputs sufficiently
rich to account for the manifest intricacy and multifarious nature of
VR-conscious experience. Additionally,
the multifocal view is encouraged by data obtained from brain ablation,
neuroimaging, and single-cell electrical recording studies, each of which has
demonstrated the importance of widely dispersed brain regions in even the
simplest VR-conscious tasks. Thus, the
ablation paradigm, by which a brain region is shown to be important for a given
task by virtue of the loss of ability to perform that task following damage to
the given brain region, has implicated brainstem, thalamic, limbic, and
widespread cortical regions in VR-conscious processing. More recently, neuroimaging studies
employing functional MRI and related imaging techniques or with those utilizing
single-cell recordings from pyramidal neurons in various brain areas have
provided direct evidence of a role for widespread cortical and subcortical
regions in VR-consciously mediated behavior (Raichle 2000).
Despite
these arguments, it remains possible that while a distributed model is
consistent with the available data, so might be a focal model. Thus, the possibility needs to be considered
that just a subset or even only one of the areas delineated in the above
studies actually mediates VR-conscious experience and that the other areas
serve merely to provide information to this single region. For example, during a VR-conscious visual
task, ablation, neuroimaging, and single-cell recording data have together
implicated activity spread across primary and secondary occipital cortices,
tertiary temporal and parietal association cortices, PFC, and multiple
diencephalic and brainstem structures in the context of VR-conscious
experience. Since, however, these
disparate regions are highly interconnected, the possibility that only one of
the identified regions actually subserves VR-conscious experience and that the
other regions serve only to provide input to this focal region cannot be
dismissed out of hand.
For a
focal model to gain serious consideration, a brain region would need to be
identified that could serve as a locus of convergence for the full set of
stimuli that feed VR-conscious experience.
Such a region should manifest certain empirically demonstrable
features. First, the area should be the
recipient of afferent connections from brain localities corresponding to each
of the sensory, emotional, and mnemonic components that make up VR-conscious
experience. Second, it should be the
case that the area is adequately connected with brain regions capable of
mediating VR-conscious behavioral output.
Third, the area should show activation with neuroimaging or single-cell
recording techniques during engagement in VR-consciously mediated tasks. And fourth, ablation of the area should
result in loss of VR-conscious experience.
In the following, the assertion will be made that there is a brain
region, namely the left lateral PFC (corresponding to portions of Brodmann
areas 9, 10, 11, 46, 47), that appears to satisfy each of the enumerated requirements.
Afferent
Connections: The first question is whether the left
lateral PFC is appropriately positioned to be the recipient of afferent
connections pertaining to each of the sensory, emotional, and mnemonic
components that comprise VR-conscious experience. A review of the neuroanatomical literature suggests that this may
indeed be the case. With regard to
sensory input, the lateral PFC has long been established to receive input from
the occipital, temporal, and parietal association cortices that process the
incoming visual, acoustic, and tactile signals that provide the organism with
information about its extrapersonal space (Kuypers et al. 1965; Pandya and
Kuypers 1969). Additionally, the
lateral PFC receives inputs from the caudal orbitofrontal cortical regions that
function as association areas for smell and taste (Baylis et al. 1995, Johnson
et al. 2000).
With
regard to emotion, ablation and activation studies have each supported a role
for both anterior cingulate and ventromedial orbitofrontal cortices in
assessing the emotional significance of stimuli (Baleydier and Mauguiere 1980,
Bush et al. 2000, Phan et al. 2002).
Anatomically, both regions are recipients of the visceral stimuli from
which emotions are proposed to be comprised (Damasio 1999) and both regions
project strongly to lateral PFC where, it is suggested (Gray et al. 2002),
emotion and cognition become integrated.
With
regard to memory, links to lateral PFC are well established for both short-term
working memory and long-term distraction-stable memory. For short-term working memory, findings from
ablation, neuroimaging, and single-cell recording studies point to the lateral
PFC as a principal site wherein information is retained for brief periods
during the performance of complex problem-solving tasks (Goldman-Rakic 1992;
D'Esposito et al. 1998; Fletcher and Henson 2001). For long-term distraction-stable memory, the lateral PFC plays a
key role in the retrieval of memories stored in posterior neocortex and
hippocampus (Goldman-Rakic 1992; Fuster 1999), and both ablation (Wheeler 1995)
and neuroimaging studies (Fletcher and Henson 2001; Braver et al. 2001,
Slotnick et al. 2003) have provided direct evidence that lateral PFC is
importantly involved in long-term memory functions.
Output
to Broca’s Area: On the efferent side, the question is
whether the left lateral PFC is able to access the motor programs that
presumably mediate VR-conscious behavioral output. Anatomically, the critical issue is whether the left lateral PFC
is connected adequately with Broca's area, the brain region that provides for
syntactical linguistic output. The
pivotal role of Broca's area, situated in the posterior part of the inferior
frontal gyrus (Brodmann's areas 44 and 45) of the left frontal lobe, in
language expression was established first in 1861 (Broca 1861) and has been
amply confirmed in the one and a half centuries that have followed. For logical, grammatical output, which is
the type involved in verbally reporting on VR-conscious experience, the
situation is asymmetric, with only the "dominant" hemisphere (the
left hemisphere in most humans and almost all right-handers) capable of
performing the function. Left lateral
PFC is ideally positioned to influence Broca's area and thereby express verbal
reports pertaining to VR-conscious experience since it lies immediately
adjacent to it and projects to it strongly (Deacon 1992).
Activation
Studies: The principal evidence for activation of the
left lateral PFC during VR-conscious tasks comes from studies of working
memory, a cognitive function that is usually regarded as VR-conscious. As noted above, neuroimaging and single-cell
recording studies indicate that lateral PFC is a principal mediating site for working
memory. Additionally, left lateral PFC
has been shown directly to become active in neuroimaging studies during tasks
involving VR-conscious experience (McIntosh et al. 1999; Kjaer et al. 2001,
Stephan et al. 2002). Event-related
potential measurements in humans have shown further that lateral PFC is
activated subsequent to posterior cortex in association with performance of
VR-conscious tasks, with a mean latency of activity over occipital areas
measured at 56 msec and over lateral PFC at 80 msec (Foxe and Simpson 2002). This temporal sequence of events would be in
keeping with a model in which posterior cortex provides preliminary processing
of stimuli for subsequent VR-conscious processing by lateral PFC.
Results
of Ablation: If the left lateral PFC were, by itself, the
mediator of VR-conscious experience, then ablation of the region should result
in its elimination. Some authors (e.g.
Taylor 2001) have cited examples, such as the celebrated case of Phineas Gage
(Damasio 1999), in which extensive prefrontal lesions have failed to eliminate
VR-conscious experience. As pointed out
by Crick and Koch (1998), however, in none of these cases has the damage
included the entirety of the lateral PFC, rendering their relevance uncertain.
On the
other hand, patients with demonstrated extensive damage to left lateral PFC
sparing Broca's area routinely exhibit the classical syndrome of transcortical
motor aphasia in which the patients are mostly mute but are still able to
mindlessly repeat phrases spoken to them.
Importantly, these patients show neither the motivation nor the ability
to spontaneously produce speech or writing or otherwise engage in behaviors
suggestive of retained VR-consciousness (Heilman and Valenstein 1993).
Such
patients do, it must be noted, continue to exhibit behavior suggestive of
residual consciousness of a non-verbally reportable variety. It is here that the reason for restricting
the initial discussion to VR-consciousness becomes apparent. The continued presence of non-verbally
reportable consciousness in these patients would be in keeping with the notion
that the brain might harbor multiple consciousnesses. In particular, the non-verbally reportable conscious behavior
evident in the transcortical motor aphasic would presumably be mediated by
structures other than the left lateral PFC.
Therefore, the contention that the damage to the left lateral PFC
resulted in a loss of VR-consciousness would not be contradicted.
To
summarize the argument thus far, while a spatially distributed model of
VR-consciousness is possible, there is evidence providing for an alternative
possibility as well: that the left
lateral PFC might by itself be the direct correlate for VR-conscious
experience. The localization to the
left lateral PFC, it should be noted, may not be the full extent to which
VR-consciousness is localized. That is,
the lateral PFC might itself be further divisible. In fact, support has been garnered for the lateral PFC
encompassing two functionally distinct subregions, one dorsolateral (portions
of Brodmann 9, 46) the other ventrolateral (portions of Brodmann 10, 11, 47),
the two subregions differing with respect to both anatomical connections and
type of information being processed (Oliveri et al. 2001). Thus, the dorsolateral PFC has been
hypothesized to work in conjunction with parietal association cortex to form a
"dorsal stream" that processes incoming information for the purpose
of sensorimotor control. The
ventrolateral PFC, on the other hand, has been proposed to join with temporal
association cortex in forming a "ventral stream" devoted to semantic
processing. Since both areas are
strongly connected to Broca's area, both are in a position to affect verbal
output. Further, since both areas are
strongly connected to each other, either could ultimately be the sole mediator
of VR-conscious experience with the other serving only to provide input to
it. In fact, Milner and Goodale (1995)
has argued for just this possibility, suggesting that only the ventral stream
is associated with VR-conscious experience and that the dorsal stream processes
information VR-unconsciously.
In the
discussion that follows, the question of which subregion by itself might
mediate VR-conscious experience will be left undecided and the generic term,
"lateral PFC," will be used to refer to the area in general. In any case, whatever the final localization
of the macroscopic anatomical substrate for VR-consciousness might be, all that
is needed for the further development of the single-neuron theory is that a
macroscopically focal correlate for VR-consciousness exists that is relatively
homogeneous and is in a position to receive all the sensory, emotional, and
mnemonic stimuli that characterize the VR-conscious experience.
4.
THE MICROSCOPIC STEP: THE SINGLE-NEURON
THEORY
Subsequent
to the question of which macroscopic brain region mediates VR-consciousness is
the question of how the neurons populating this region accomplish the
task. According to the generally
accepted view, the participating neurons join their activity into a single VR-conscious
experience via nonlinear dynamic mechanisms.
The single-neuron theory posits, instead, that a subpopulation of
neurons in the region, rather than joining their activity into a single
VR-consciousness, remain separately VR-conscious and produce the illusion of a
joint VR-consciousness by virtue of the summation of their output. In the model, each of the VR-conscious
neurons is proposed to experience not merely a fragment of a higher-order joint
VR-consciousness but, rather, the whole range and complexity of VR-conscious
experience generally attributed to the population as a whole. Specifically, these neurons would be assumed
to have the following properties:
a) The
activity of each pyramidal neuron in the subpopulation independently serves as
an NCC for the entire content of VR-conscious experience.
b) Each of
the pyramidal neurons in the subpopulation mediates approximately the same
conscious content as do all the others.
c) The
output from each of the pyramidal neurons carries approximately the same
frequency-encoded longitudinal message as do all the others.
d) Just
which pyramidal neurons comprise the subpopulation, as well as how numerous
they are, will need to be determined empirically, provided the overall theory
proves to be valid.
The
neurons mediating VR-consciousness in this model would be assumed to be a
subgroup of pyramidal neurons, which are by far the predominant neuronal type
in the cortex in general and in the lateral PFC in particular (Abeles, 1991). For the single-neuron theory to be possible,
these neurons would have to satisfy at least four conditions. First, they would need to be individually
complex enough on the input side to support the complexity of VR-conscious
experience. Second, they would
individually need to be recipients of each of the kinds of inputs that make up
the VR-conscious experience. Third,
they would need to be able to produce sufficiently complex output to account
for the complexity of VR-conscious behavior.
Fourth, their outputs would need to be capable of being summated in such
a manner that the individual signals would be synchronized and amplified so as
to yield the appearance of a single macroscopic VR-consciousness. A review of
the anatomy and physiology of the lateral PFC suggests that these conditions
might be satisfied for this brain region.
Complexity
of Inputs to Pyramidal Neurons: The principal point here
is that cortical pyramidal neurons receive a huge number of afferent signals
over their dendritic trees. It is
estimated that for humans each cortical pyramidal neuron incorporates
approximately 40,000 synapses within its dendritic tree (Abeles 1991), a number
larger than is usually appreciated and one that allows for an impressive
complexity of information encoding. For
example, if only one tenth of one percent of the synapses of a cortical
pyramidal neuron were assumed to participate in a given VR-conscious
experience, and if only a simple binary code were being used (that is, one in
which the synapse is either active or inactive), then 240 or about
one trillion different patterns could be encoded by that neuron.
An
alternative calculation, also focusing on single neuron transmission capacity,
has been made by Bieberich (2002) in his presentation of a theory not unlike
the one postulated here. According to
Bieberich, if it is assumed that 5,000 simultaneously arriving synaptic input
bytes, corresponding to 5,000 active spines in the dendritic tree, are turned
over with a frequency of 50 Hz and a compression factor of 20, then a single
neuron would be capable of processing 5 mB of information per second. This, he argues, constitutes a rate of
information processing adequate to plausibly account for the complexity of
VR-conscious experience.
By either
of these calculations, individual cortical pyramidal neurons appear capable of
processing information of a complexity greater than often appreciated, and
quite possibly complex enough to mediate the entirety of the VR-conscious
experience.
Convergence
of Inputs Upon Individual Pyramidal Neurons: The question here is, if
the lateral PFC as a whole receives all of the inputs that comprise
VR-conscious experience, then is it plausible that at least some of the
individual pyramidal neurons within the region do likewise? That is, is it plausible that the
information that converges upon the region as a whole converges, in holographic
fashion, separately and redundantly on each of a subgroup of pyramidal neurons
populating the region? In support of the
presence of such an arrangement is the clinical observation that focal lesions
within lateral PFC do not result in modality-specific deficits but only
diminish the region's function in a general manner. This suggests at least some degree of microscopically redundant
convergence throughout the extent of the region. Additionally, individual cortical neurons typically receive
inputs from thousands of other neurons (Koch 1997, Schuz 1998) and so are in a
position to serve as nodes of converging information. Aside form general considerations, however, are the reports that
direct single-cell recordings have identified neurons in lateral PFC that
respond selectively to conjoint visual and auditory stimuli (Aou et al. 1983),
to conjoint visual, auditory and tactile stimuli (Tanila et al. 1992), and to
conjoint object and location features (Rao et al. 1997). Whether a subgroup of
lateral prefrontal neurons exists in which each neuron in the subgroup receives
convergent input from all the sensory, emotional, and mnemonic stimuli that
comprise VR-conscious experience is yet to be empirically determined.
Amplification
of Output: If the single-neuron theory is correct and
conscious experience corresponds to the activity of single neurons, then some
method of amplification would be necessary for the output of the individual
neurons to have macroscopic behavioral consequences. In fact, a simple mechanism of amplification may be available if
it can be assumed that, at any given moment, each of the neurons subserving VR-consciousness
emits via its exiting axon more or less the same output as do all of the
others. This, in turn, would follow if
it could be postulated that, at any given moment, each of the neurons
subserving VR-consciousness receive more or less the same input as do all the
others.
Consideration
of the relevant microanatomy suggests that these assumptions may not be
unreasonable. To begin with, with
regard to input, some of the parallel axons arriving from posterior neocortex
or from subcortical regions may already be carrying duplicate messages if, as
is commonly assumed, redundancy of information encoding is a characteristic
feature of information processing in the brain in general. Additionally, axons projecting to PFC
arborize on approaching their targets, with single axons innervating hundreds
or thousands of different post-synaptic targets (Weinberg et al. 1990, Gilbert
1998, Schuz 1998). The result is that
the same input signals are likely to be distributed redundantly to a
considerable number of pyramidal neurons in the targeted lateral PFC. If, additionally, the relative weightings of
the synaptic inputs can be assumed to be similar across neurons (an assumption
that will need to be empirically examined), and if the neurons can be assumed
to respond similarly upon receiving similar inputs, then the outputs emerging
from these neurons might reasonably be expected to be similar as well. Such would, in fact, be consistent with
reports that single-cell recordings obtained simultaneously from multiple
lateral prefrontal pyramidal neurons during tasks involving working memory have
revealed significant cross-correlations of the emitted signals among at least
some of the neurons in the subgroups examined (Funahashi and Inoue 2000,
Constantinidis et al. 2001).
The
amplification procedure thus described would be analogous to that which occurs
when a crowd watches fireworks. With
every pyrotechnic explosion, each individual in the crowd verbalizes his or her
own reaction with an "ooh" or an "aah." While the individual outputs may not be
audible at a distance, the collected vocalization of all the members of the
crowd would be. In analogy with the
single-neuron model, the individuals would be responding separately to the
stimulus but the group would appear to be responding as a whole. In the brain, however, it would be Broca's
area (and other effector frontal cortical areas) that would "hear"
the amplified message emitted by the neurons in the left lateral PFC.
The
mechanism of summation of output would provide not only for amplification of
the outgoing message but also for the elimination of sporadic errors produced
by stray neurons. This error-control
procedure would be analogous to that which occurred in 1999 when Gary Kasparov,
the then reigning world chess champion, played a game of chess with "the
world" over the internet.
Thousands of chessplayers, analogous to the thousands of VR-conscious
neurons in the left lateral PFC, participated.
Players were hooked into a central node through which they each received
Kasparov's moves and were able to submit their own replies. The move selected by the largest number of
respondents was chosen as "the world's" reply. The resulting game was of high quality (which,
incidentally, Kasparov won). From
Kasparov's point of view, he was playing a single opponent whose moves included
both short-term tactical and long-term strategic motifs. In fact, he was playing a population of
humans comprising individuals who separately perceived and calculated their
moves but with final options chosen according to the majority opinion. The arrangement resulted in a performance by
"the world" that was at a higher level than would have been produced
by any one player acting alone. This
was the case because sporadic blunders were ignored by the selection process,
just as sporadic errors produced by stray neurons are ignored with the
single-neuron theory.
If the
neurons in the lateral PFC did, in fact, summate their outputs according to a
"majority-rule" mechanism, then what of the experience of the
minority neurons? Would they not be
surprised and perplexed at behavioral output that was at odds with what they
intended? In fact, such would be the
case only if these neurons were capable of having direct knowledge of their
prior intentions. According to the
single-neuron theory, however, experience is determined solely by the inputs a
neuron receives via its dendrites and, since a neuron does not send recurrent
axonal collaterals back to its own dendritic tree (Abeles 1991), these bring in
group information only. A single
neuron, then, whether a member of the majority or a member of the minority,
would be expected to equate its own prior intention with that of the
group. A similar mechanism may, in
fact, contribute to the pervasiveness of the intuition that one's VR-conscious
experience in general is associated with the neuronal population rather than
with a single neuron.
Complexity
of Output: The key here is that the complexity of
neuronal output associated with VR-conscious behavior is a manifestation of the
integration of signals over time, rather than of their integration over
space. Indeed, VR-conscious
decision-making has been argued to be a low-capacity, single-channel process in
which only about one to sixteen bits of information are processed per second
(Edelman and Tononi 2000). Yet, despite
this limitation in capacity per unit time, the overall complexity that can be
achieved by integrating successive signals longitudinally can be enormous. Thus, even a Shakespearean play can be
reduced to a longitudinal sequence of binary signals. According to empirical investigation, longitudinal rather than
cross-sectional integration of information has, in fact, been found to underlie
many brain functions, including such diverse activities as eye movement, navigation,
short-term memory of continuous variables, and mental rotation (Pouget and
Latham 2002). The assumption made in
the single-neuron theory is that longitudinal integration accounts for the
complexity of the messages emitted by the VR-conscious neurons in the lateral
PFC.
In
summary, a case has been made for the possibility that, at the microscopic
level, VR-consciousness is mediated by single neurons rather than by a neuronal
population. The macroscopic step was
necessary to provide for individual neurons that receive all the inputs
comprising VR-conscious experience and for the supposition that there might be
groups of such neurons that individually receive similar input. In the microscopic step, it was argued
additionally that individual neurons are by themselves sufficiently complex to
account for the complexity of VR-conscious experience and that a simple
mechanism of summation of output might be available that could achieve both
signal amplification and error control.
5.
ADDITIONAL CONSIDERATIONS:
Other
Conscious Regions: The discussion so far has been limited to
the case of VR-consciousness, that form of consciousness largely responsible
for the debate over the "hard" problem of consciousness. It was necessary to invoke this restriction
in view of the clinical observation that patients with lesions that destroy
VR-consciousness appear to manifest a residual form of non-verbal
consciousness. The presence of such
cases raises the possibility that there are brain regions that mediate forms of
consciousness that are not verbally reportable. Damasio (1999) has argued for just such a possibility, suggesting
that there are two overlapping types of consciousness, a non-verbal "core
consciousness," mediated by midline cortical and subcortical structures,
and a verbal "extended consciousness," mediated by lateral
neocortical structures. The notion that
a single brain might subserve multiple centers of consciousness has been
suggested by other investigators as well (Geschwind 1981, Edelman and Tononi 2000).
A
particularly intriguing possible center of non-verbal consciousness is that
potentially associated with the right lateral PFC. Since this region is
anatomically homologous to the left lateral PFC, being distinguished from the
latter principally by its lack of direct connections with Broca's area, it
might be possible that it mediates a non-verbal form of consciousness separate
from that mediated by the left hemisphere.
In 1973, Rolando Puccetti suggested exactly this possibility (Puccetti
1973), proposing that the apparent duplication of consciousness that results
from corpus callosum resection (the so-called "split-brain"
procedure) is best explained by assuming that the right and left hemispheres
maintain separate conscious streams not only after callosal disconnection but
before the disconnection as well.
According to his hypothesis, the callosal section merely serves to
uncouple what are already, in the normal state, two anatomically separate
consciousnesses. Such a notion would
fit well with the single-neuron theory, which readily admits to the existence
of multiple anatomically separate centers of conscious experience.
In
Puccetti's model, it should be noted, the hypothesis is that there are no more
than two conscious centers present, and the discussion is limited to the
macroscopic level only. With the
presently proposed theory, an additional step is taken, that of proposing that
many macroscopic conscious centers may be present in a single brain, and that
the multiplicity of consciousnesses extends to the microscopic single-neuron
level as well. The overall picture
would be one in which multiple macroscopic centers of consciousness are
proposed to exist, including ones located throughout neocortical, subcortical,
and brainstem regions, with each center composed, in turn, of populations of
neurons that individually and redundantly mediate the conscious activity
appropriate to the brain region within which they reside.
Other
Single-Neuron Models: Comparison of the single-neuron theory with
other models that focus on single neurons may help clarify just what the
single-neuron theory does and does not propose. For example, it is important to distinguish the function of the
single neurons in the single-neuron theory from those referred to as
"grandmother cells," single neurons whose activation corresponds to
the experience of a single memory (Thorpe 1998). The grandmother cell concept has in common with the single-neuron
theory the notion that a single neuron may contain sufficient complexity to
account for the complexity of a complete conscious experience. It differs, however, in that the grandmother
cell is assumed, in the context of explaining memory function, to be forever
attached to a single experience, whereas the single neurons of the
single-neuron theory flexibly change their experiences over time. Among other consequences of this
distinction, the limitations in processing capacity that plague grandmother
cell models do not apply to the single-neuron theory.
Another
single-neuron based model was described by William James (1890) in his
discussion of what he called the "theory of polyzoism or multiple
monadism." According to this view,
"every brain-cell has its own individual consciousness, which no other
cell knows anything about, all individual consciousnesses being 'ejective' to
each other." Along similar lines,
Zeki and Bartels (1999) have recently proposed that a primate visual brain
consists of many separate functionally specialized processing systems
comprising hierarchical nodes that each generate a
"microconsciousness." Neither
of these schemes, however, explains how the individual microconsciousnesses are
able to induce macroscopically evident behavior. Zeki attempts to solve this problem by suggesting that the many
microconsciousnesses participate in a higher order integrative activity that
produces macroscopic consciousness.
This, however, returns us to the received view that consciousness is
ultimately mediated by multiple neurons linked through nonlinear dynamic mechanisms. James, on the other hand, considers the
possibility that a single pontifical arch-cell by itself mediates the totality
of one's consciousness but he goes on to assert that there is no evidence for
such a single "center of gravity" in the brain. Both authors appear to overlook the
possibility that multiple separately and redundantly conscious neurons might
summate their outputs so as to produce the illusion of a single mind.
Only one
other author has proposed a model comparable to the one being offered
here. Thus, Bieberich (2002) has
proposed a "recurrent fractal neural network" model in which
information at the network level is reflected at the single neuron level. As with the single-neuron theory being
proposed in the present paper, the individual neurons in Bieberich's model are
also assumed to mediate the entirety of a subject's conscious experience at a
given moment. No specific anatomical
representation is described, however.
Bieberich's model is, rather, intended as a framework for theories of
consciousness at the single neuron level; the single-neuron theory proposed
here can be seen as offering a specific neuroanatomical instantiation of
Bieberich's general framework.
The
Single-Neuron Theory and the Binding Problem: The most immediate
implication of the single-neuron theory is that it provides a novel way of
tackling the "binding problem," the problem of accounting for the
apparent unity of conscious experience.
According to the currently popular view, which attempts to solve the
binding problem in the context of an anatomically distributed model of
consciousness, the expectation is that nonlinear dynamical mechanisms,
including those associated with 40 Hz gamma frequency electrical oscillations,
will ultimately resolve the difficulty.
In contrast, the single-neuron theory offers an alternative possibility,
that binding may be achieved by anatomical convergence. That is, if it were true that single neurons
were present that received the full complement of inputs that comprise conscious
experience, then perceptual binding might be achievable on the basis of
convergence of input upon individual neurons.
In such a model, topographical convergence rather than temporal
synchrony would be invoked to explain perceptual unity. Of course, a mechanism would then be needed
to explain binding within neurons, which, as William James noted over a century
ago (James 1890), are themselves aggregates of individual particles. But at least the venue would be changed,
with the search for a mechanism of binding being transferred from the neural
network level to that within the single neuron.
It must be
noted that the above presupposes that the apparent unity of conscious
perception is a real phenomena. It is
possible, instead, that, as has been asserted by Dennett (1991) and others,
perceptual unity is an illusion. It is
possible, that is, that our apparently unified experience actually consists of
independent fragments, and that the fragments never combine into a single
experience. If such were only partially
the case, with the fragments being themselves composed of convergent elements,
then there would still be a role for the single-neuron theory arrangement in
explaining the partial convergence. But
if the extreme situation were present, in which each and every component of
what seems to be a unified experience were associated with the activity of a
different neuron, then the single-neuron theory proposed here would be rendered
trivial. Instead, Dennett's approach to
explaining consciousness would suffice.
What is
needed to resolve this issue is a better understanding of the process of
introspection, the principal source of our intuition that perceptual unity is
real. It is possible, for example, that
our introspective intuition is entirely faulty, and that perceptual unity is an
illusion. On the other hand, it is
possible that our introspective intuition accurately reflects the true nature
of our conscious experience, and that perceptual unity is real. The relevance of the convergent single-neuron
solution to the binding problem hinges on which of these alternatives is
valid. Until a comprehensive theory of
introspection is available, however, the degree to which perceptual unity
represents a real phenomenon must be considered undecided.
Empirical
Predictions: There are a number of testable predictions
made by the single-neuron theory, the presence of which serves to distinguish
it from the competing network theories of consciousness. To begin with, the single-neuron theory
makes the anatomical prediction that pyramidal neurons will be found in the
left lateral PFC that are individually the recipients of convergent axonal
input derived from brain regions considered to be involved in the processing of
the sensory, mnemonic, and emotional stimuli that compose VR-conscious
content. In addition, the theory makes
the electrophysiologic prediction that left lateral PFC neurons will be found
that respond in single-cell recording experiments to combinations of stimuli
that typically comprise VR-conscious experience. As noted above, direct single-cell recordings have already
identified neurons in lateral PFC that respond selectively to conjoint visual
and auditory stimuli (Aou et al. 1983), to conjoint visual, auditory and
tactile stimuli (Tanila et al. 1992), and to conjoint object and location
features (Rao et al. 1997). The
question is whether lateral PFC neurons exist that respond to conjoint input
from the full complement of sensory, emotional, and mnemonic stimuli that
comprise VR-conscious experience. The
demonstration of the existence of neurons that are suitably anatomically and
electrophysiologically convergent, while expected with the single-neuron
theory, would be difficult to justify within the network NCC framework. Alternatively, the failure to identify such
neurons despite a concerted effort to do so would militate against the
single-neuron theory and favor the network approach.
An
additional prediction of the single-neuron theory would be that subgroups of
lateral PFC neurons will be found that share similar inputs and that emit more
or less the same message over their exiting axons. Data from simultaneous single-cell recordings taken from multiple
lateral prefrontal neurons have in fact already been reported that show
significant cross-correlations among groups of PFC neurons during the
performance of conscious tasks (Funahashi and Inoue 2000, Constantinidis et al.
2001). It would be the expectation of
the single-neuron theory that further work with these cross-correlations will
suggest the presence of a common message being emitted redundantly by these
neurons, and that, as suggested by Nirenberg and Latham (2003), the correlated
component of the signals might serve as an "extra information
channel" that itself might correlate with conscious behavioral output.
Speculative
Implications: As so far presented, the single-neuron
theory does no more than shift the locus of the mind/brain interface from the
neural network to the single neuron level of information processing. It does not, by itself, offer any
fundamental advance in tackling the philosophical difficulties inherent in the
problem. That is, the theory as so far
presented does not take on the deeper questions of how and why individual
neurons are imbued with experience. It
might, though, be possible to extend the theory in a way that does address
these deeper questions. In particular,
since the mind/brain interface has been shifted to the level of the single
neuron, certain physical processes, such as those involving electromagnetic
fields or quantum mechanical phenomena, might be more plausibly invoked in
theories of mind/brain interaction since the need to explain how these
phenomena "jump" across synaptic spaces can be avoided. Inclusion of such phenomena in evolving
mind/brain theories might, in turn, offer a degree of flexibility that could
allow such theories to address the deeper philosophical issues.
As an
example of how this might work, I offer the following brief speculative sketch
derived from Whitehead's panpsychist approach to the hard problem of
consciousness. According to Whitehead
(1933), the basic stuff of the universe is neither subjective experience nor
objective matter but neutral "occasions" (or "events") that
appear as either subjects or objects depending on one's observational
perspective. Thus, the same event is a
subject with respect to the information it receives (that is, it
"perceives" the incoming information) but is an object with respect
to the information it emits (and which is subsequently "perceived" by
other events). In Whitehead's view,
mind/brain duality is just a complex macroscopic instance of the perspectival
duality that pervades all of nature.
The
difficulty with Whitehead's formulation is that it lacks a convincing explanation
of how simple subject/object events combine to form complex subject/object
entities such as those embodied by human minds. Seager (1995) has called this difficulty the "combination
problem." Why do some
configurations of matter (such as human brains) appear to serve as complex but
unified subject/object entities, while others (such as rocks and thermostats)
remain as mere aggregates of elementary subject/object events? Seager suggests that only the synthetic
nature of quantum mechanics, especially the phenomenon of quantum entanglement
(in which spatially distributed occurrences are joined into a single event at
the moment of reduction of the state vector), appears capable of resolving the
combination problem.
The
possible involvement of quantum mechanics in consciousness has been summarily
dismissed by many authors because the entanglement would, it is usually
supposed, have to extend across macroscopic distances and involve spatially
dispersed neuronal populations. The
difficulties imposed by such large distances, together with the lack of a
plausible mechanism by which entanglement might "jump" across
synapses, has been argued to render quantum mechanical theories of
consciousness untenable (Grush and Churchland 1995). With the single-neuron theory, however, the proposed entanglement
would need to extend only throughout a portion of the dendritic tree of a
single neuron. While still a formidable
proposition, the speculation that quantum mechanical effects might be relevant
to consciousness might nevertheless gain in plausibility.
The
specific way that quantum entanglement could be invoked to explain
consciousness would be as follows.
Suppose that within the dendritic tree of the neuron there were
indivisible entangled events whose topology were reflective of the
temporospatial patterns of electrical activity within the larger dendritic
tree. It might be possible that such
entangled events could individually be recipients of all the stimuli that go
into conscious experience and be complex enough to match the complexity of
conscious experience. If such entangled
events existed, then populations of them could conceivably summate their
outputs and affect the neuron's outgoing message in a manner analogous to that
in which, on the macroscopic level, populations of neurons are proposed to
summate their outputs and affect Broca's area.
As has
been noted by Bieberich, who has articulated an argument similar to the one
being offered here (Bieberich 2002), entangled intraneuronal events could
conceivably support a complexity of information processing comparable to that
attributable to the whole brain in the neural network models. Such entangled events could, in turn, act as
indivisible Whiteheadean subject/object entities with subjective aspects serving
as units of conscious experience and with objective aspects contributing to the
information content of outgoing electrochemical messages at the axon
hillock. In the final model, then, a
single subjective experience would correspond not to the activity of a single
neuron but to the occurrence of a single entangled event within a single
neuron. In a logical extension of the
single-neuron theory, an individual's brain would be construed as comprising a
multiplicity of subjective experiences corresponding not just to the multitude
of neurons within that brain, but to the larger number of entangled events
within all those neurons. In sum, the
combination problem would be solved by avoiding altogether the need to combine
the individual consciousnesses.
This process
would be assumed to be occurring not only in the right and left lateral
prefrontal cortical neurons but in other neurons as well and even more
generally throughout nature. That is,
every quantum mechanical event in the universe would be considered to manifest
subjective/objective duality. What
would elevate a given quantum event to the status of a macroscopically
observable conscious entity would be the manner in which it was coupled with
input and output. Thus, quantum
mechanical events found generally in nature might well act as Whiteheadean
subject/object entities but would have inputs and outputs reflecting only their
immediate ultramicroscopic environments.
Events within the lateral PFC, in contrast, would be connected with
inputs and outputs attached to happenings in the far-removed macroscopic world.
There are,
of course, serious challenges to this scheme, not the least of which is the
need to demonstrate that there exist quantum mechanically entangled events
spatially dispersed enough to invade at least several dendritic branches. The assumptions are, however, empirically
testable in principle. The quantum
mechanical model is offered, in any case, principally to illustrate how the
transfer of the locus of mind/brain interaction to the intraneuronal domain
might bring into play physical processes that would otherwise be generally
regarded as irrelevant.
6.
SUMMARY:
A model of
mind/brain interaction has been outlined that places the mind/brain interface
at the level of single neurons or even at the level of single quantum events
within neurons. The scheme is built on
the combined premise that there are subgroups of neurons that (1) individually
receive all the types of inputs that characterize conscious experience, (2) are
sufficiently complex on the input side to match the complexity of conscious
experience, (3) produce complex output by means of longitudinal integration of
their axonal outputs, and (4) summate their outputs to achieve amplification
and error control. It is not argued that
this model is necessitated by the available data, only that it is compatible
with them.
Ultimately,
further empirical investigation into the behavior of single neurons will
determine whether the model is valid.
Specifically, the theory predicts the presence of subgroups of lateral
prefrontal neurons that share similar inputs, that individually show responses
in single-cell recording experiments to all the stimuli that comprise verbally
reportable conscious experience, and that are sufficiently numerous to allow
for adequate amplification and error control.
The theory also predicts that continued examination of data obtained
from simultaneous single-cell recordings taken from multiple lateral prefrontal
neurons will serve to replicate and extend the preliminary reports of
significant cross-correlations among subgroups of such neurons during the
performance of conscious tasks, such that the correlated component of the
signals might even serve as an "extra information channel" (Nirenberg
and Latham 2003) that itself might correlate with conscious behavioral
output. The presence of these specific
predictions, it is argued, renders the theory potentially falsifiable, and
therefore of a legitimately scientific nature.
The idea
that single neurons might be individually conscious was originally considered
by William James (1890) who went on, however, to note that "the cell is no
more a unit, materially considered, than the total brain is a unit. It is a compound of molecules, just as the
brain is a compound of cells and fibers.
And the molecules, according to the prevalent physical theories, are in
turn compounds of atoms." A
single-neuron theory would, then, still have to explain how the atoms of a
neuron combine to form a single consciousness.
In response to this issue, and to illustrate the way in which the
transfer of mind/brain interaction to the intraneuronal domain might facilitate
the development of models of mind/brain interaction, a speculative sketch was
offered that was built upon Whitehead's panpsychist approach to the mind/brain
problem. Specifically, it was
postulated that entangled quantum mechanical events within neurons might serve
as indivisible Whiteheadean subject/object entities of sufficient complexity
and connectedness to allow them to individually mediate the totality of
conscious experience usually attributed to the brain as a whole. The individual consciousnesses attached to
single events would, in this picture, not combine but would instead remain
independently conscious, thereby solving the combination problem by avoiding it
altogether. Such an extension of the
single-neuron theory would, admittedly, be highly speculative but it would
provide an example of how the theory might offer more than just an alternative
model of cerebral information processing and go the further step of addressing
the fundamental problem of mind/brain interaction itself.
ACKNOWLEDGMENTS:
I wish to
thank Josef Ashkenazi, Ph.D, Associate Professor of Physics, University of
Miami, for his help in developing the ideas pertaining to quantum
mechanics. I also wish to thank
Mohammad Rahat, David Wilson, Robert Fujimora, Mihai Preda, Gloria Peruyera,
Todd Feinberg, and Kenneth Heilman for their valuable comments and suggestions.
REFERENCES:
Abeles M, 1991:
Corticonics: Neural Circuits of the Cerebral Cortex. New York:
Cambridge
University Press.
Aou S,
Oomura Y, Hishino H, Ono T, Yambe K, Sikdar SK, Noda T, Inoue M, 1983:
Functional heterogeneity of single neuronal activity in the monkey dorsolateral
prefrontal cortex. Brain Res 260:121-124.
Baleydier
C, Mauguiere F, 1980: The duality of the cingulated gyrus in monkey.
Neuroanatomical study and functional hypothesis. Brain 103:525-554.
Baylis LL,
Rolls ET, Baylis GC, 1995: Afferent connections of the caudolateral
orbitofrontal cortex taste area of the primate. Neuroscience 64:801-812.
Bieberich
E, 2002: Recurrent fractal neural networks: a strategy for the exchange of
local and global information processing in the brain. BioSystems 66:145-164.
Braver TS,
Barch DM, Kelley WM, Buckner RL, Cohen NJ, Miezin FM, Snyder AZ, Ollinger JM,
Akbudak E, Conturo TE, Petersen SE, 2001: Direct comparison of prefrontal
cortex regions engaged by working and long-term memory tasks. Neuroimage
14:48-59.
Broca P,
1861: Perte de la parole, remollissement chronique et destruction partielle du
lobe anterieur gauche du cerveau. Bull Soc Anthropol 2:235-238.
Bush G,
Luu P, Posner MI, 2000: Cognitive and emotional influences in anterior
cingulated cortex. Trends in Cognitive Science 4:215-222.
Chalmers
D, 1996: The Conscious Mind. New York: Oxford University Press.
Constantinidis
C, Franowicz, Goldman-Rakic PS, 2001: Coding specificity in cortical
microcircuits: a multiple-electrode analysis of primate prefrontal cortex. The
Journal of Neuroscience 21:3646-3655.
Crick F,
Koch C, 1998: Consciousness and Neuroscience. Cerebral Cortex 8:97-107.
Damasio
AR, 1999: The Feeling of What Happens. Harcourt Brace and Company: New York.
Deacon TW,
1992: Cortical connections of the inferior arcuate sulcus cortex in the macaque
brain. Brain Research 573:8-26.
Dennett
DC, 1991: Consciousness Explained. Boston: Little, Brown and Company.
D'Esposito
M, Aguirre GK, Zarahn E, Ballard D, Shin RK, Lease J, 1998: Functional MRI
studies of spatial and nonspatial working memory. Cognitive Brain Research
7:1-13.
Edelman GM
and Tononi G, 2000: A Universe of Consciousness: How Matter Becomes
Imagination. New York: Basic Books.
Fletcher
PC, Henson RNA, 2001: Frontal lobes and human memory: insights from functional
neuroimaging. Brain 124:849-881.
Foxe JJ,
Simpson GV, 2002: Flow of activation from V1 to frontal cortex in humans. A
framework for defining "early" visual processing. Exp Brain Res
142:139-150.
Funahashi
S, Inoue M, 2000: Neuronal interactions related to working memory processes in
the primate prefrontal cortex revealed by cross-correlation analysis. Cerebral
Cortex 10:533-551.
Fuster JM,
1999: Memory in the cerebral cortex. MIT Press: Cambridge.
Geschwind
N, 1981: The perverseness of the right hemisphere. The Behavioral and Brain
Sciences 4:106-107.
Gilbert
CD, 1998: Adult cortical dynamics. Physiological Reviews 78:467-485.
Goldman-Rakic
PS, 1992: Working memory and the mind. Scientific American September.
Gray JR,
Braver TS, Raichle ME, 2002: Integration of emotion and cognition in the
lateral prefrontal cortex. PNAS 99:4115-4120.
Grush R,
Churchland PS, 1995: Gaps in Penrose's toilings. J of Consciousness Studies
2:10-29.
Hardcastle
V, 1994: Psychology's binding problem and possible neurobiological solutions. J
of Consciousness Studies 1:66-90.
Heilman
KM. and Valenstein EV, 1993: Clinical Neuropsychology. New York: Oxford
University Press.
James W, 1890:
Principles of Psychology. Cambridge: Harvard University Press.
John ER,
2001: A field theory of consciousness. Consciousness and Cognition 10:184-213.
Johnson
DMG, Illig KR, Behan M, Haberty LB, 2000: New features of connectivity in
piriform cortex visualized by intracellular injection of pyramidal cells
suggest that "primary" olfactory cortex functions like
"association" cortex in other sensory systems. The Journal of
Neuroscience 20:6974-6982.
Koch C,
1997: Computation and the single neuron. Nature 385:207-210.
Kjaer TW,
Nowak M, Kjaer KW, Lou AR, Lou HC, 2001: Precuneus-prefrontal activity during
awareness of visual verbal stimuli. Consciousness and Cognition 10:356-365.
Kuypers
HGJM, Szwarcbart MK, Mishkin M, 1965: Occipitotemporal cortico-cortical
connections in the rhesus monkey. Expl
Neurol 11:245.
McIntosh
AR, Rajah MN, Lobaugh NJ, 1999: Interactions of prefrontal cortex in relation
to awareness in sensory learning. Science 284:1531-1533.
Milner AD,
Goodale MA, 1995: The Visual Brain in Action. Oxford University Press: Oxford.
Nirenberg
S, Latham PE, 2003: Decoding neuronal spike trains: How important are
correlations? PNAS 100:7348-7353.
Oliveri M,
Purriziani P, Carlesimo GA, Koch G, Tomaiuolo F, Panella M, Caltagirone C,
2001: Parieto-frontal interactions in visual-object and visual-spatial working
memory: evidence from transcranial magnetic stimulation. Cerebral Cortex
11:606-618.
Pandya DN,
Kuypers HG, 1969: Cortico-cortical connections in the rhesus monkey. Brain
Research 13:13-48.
Phan KL,
Wager T, Taylor SF, Liberzon I, 2002: Functional neuroanatomy of emotion: a
meta-analysis of emotion activation studies in PET and fMRI. Neuroimage
16:331-348.
Pouget A,
Latham P, 2002: Digitalized neural networks:
long-term stability from forgetful neurons. Nature Neuroscience
5:709-710.
Puccetti
R, 1973: Brain bisection and personal identity. British Journal of Philosophy
of Science 24:339-355.
Raichle
ME, 2000: The neural correlates of consciousness: an analysis of cognitive skill
learning. In Gazzaniga MS: The New Cognitive Neurosciences, Second Edition, MIT
Press: Cambridge.
Rao SC,
Rainer G, Miller EK, 1997: Integration of what and where in the primate
prefrontal cortex. Science 276:821-824.
Revonsuo
A, 1999: Binding and the phenomenal unity of consciousness. Consciousness and
Cognition 8:178-185.
Schuz A,
1998: Neuroanatomy in a computational perspective. In Arbib MA: Handbook of
Brain Theory and neural Networks. MIT
Press: Cambridge.
Seager W,
1995: Consciousness, information and panpsychism. Journal of Consciousness
Studies 2:272-288.
Slotnick
SD, Moo LR, Segal JB, Hart J, 1969: Distinct prefrontal cortex activity
associated with item memory and source memory for visual shapes. Cognitive
Brain Research 17:75-82.
Sperry RW,
1969: A modified concept of consciousness. Psychological Reviews 26:532-536.
Stephan
KM, Thaut MH, Wunderlich G, Schicks W, Tian B, Tellmann L, Schmitz T, Herzog H,
McIntosh C, Seitz RJ, Homberg V, 2002: Conscious and subconscious sensorimotor
synchronization - prefrontal cortex and the influence of awareness. Neuroimage
15:345-352.
Tanila H,
Carlson S, Linnankoski I, Lindroos F, Kahila H, 1992: Functional properties of
dorsolateral prefrontal cortical neurons in awake monkey. Behav Brain Res 47:169-180.
Taylor JG,
2001: The central role of the parietal lobes in consciousness. Consciousness
and Cognition 10:379-417.
Thorpe S,
1998: Localized versus distributed
representations. In: Arbib MA: Handbook
of Brain Theory and Neural Networks. MIT Press: Boston.
Weinberg
RJ, Pierce JP, Rustioni A, 1990: Single fiber studies of ascending input to the
cuneate nucleus of cats: I. Morphometry of primary afferent fibers. J Comp
Neurol 300:113-133.
Wheeler
MA, Stuss DT, Tulving E, 1995: Frontal lobe damage produces episodic memory
impairment. Journal of the International Neuropsychological Society 1:525-536.
Whitehead
AN, 1933: Adventures of Ideas. New York: The Free Press.
Zeki S,
Bartels A, 1999: Toward a theory of visual consciousness. Consciousness and
Cognition 8:225-259.
[1] The designation "left hemisphere" will be used to refer to the "dominant" or "language" hemisphere, located on the left side of the brain in most people.