SINGLE-NEURON THEORY OF CONSCIOUSNESS
Departments of Psychiatry and Neurology
University of Miami School of Medicine
1400 NW 10 Ave, Suite 702
Miami, Florida 33136
This work was presented in abstract form at
"Toward a Science of Consciousness" held in Tucson, April 2002.
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.
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 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.
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.
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.
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 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.