The liabilities of mobility: A selection pressure for the transition to consciousness in animal evolution

Consciousness and Cognition Consciousness and Cognition 14 (2005) 89–114 www.elsevier.com/locate/concog

The liabilities of mobility: A selection pressure for the transition to consciousness in animal evolution Bjorn Merker* Department of Psychology, Uppsala University, SE-75142, Sweden Received 12 March 2002 Available online 20 February 2003

Abstract The issue of the biological origin of consciousness is linked to that of its function. One source of evidence in this regard is the contrast between the types of information that are and are not included within its compass. Consciousness presents us with a stable arena for our actions—the world—but excludes awareness of the multiple sensory and sensorimotor transformations through which the image of that world is extracted from the confounding influence of self-produced motion of multiple receptor arrays mounted on multijointed and swivelling body parts. Likewise excluded are the complex orchestrations of thousands of muscle movements routinely involved in the pursuit of our goals. This suggests that consciousness arose as a solution to problems in the logistics of decision making in mobile animals with centralized brains, and has correspondingly ancient roots. Ó 2003 Elsevier Inc. All rights reserved. Keywords: Consciousness; Phylogeny; Centralized brain plan; Decision mechanisms; Zona incerta; Neuroepistemology

1. Introduction There is currently no consensus regarding the nature and function of consciousness. Proposals cover a wide range of constructs. At one end of this spectrum consciousness may be cast in a privileged relation to human language (Macphail, 1998, 2000), while at the other it is construed as a fundamental feature of the world on a par with mass, charge, and space-time (Chalmers, 1995,

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1996). The explanandum itself is ill defined, in other words. In such a situation specific conjectures regarding the nature, function or origin of consciousness have a special role to play by providing a focus for attempts to determine the extent to which they fit available facts. In what follows one such specific proposal will be elaborated. Consciousness will be interpreted as a biological function evolved by mobile animals as a solution to neural logistics problems inherent in the control of orientation to their surroundings. The interpretation is motivated by the conspicuous absence from the contents of consciousness of two significant classes of information known to be present in brains, one on the afferent and the other on the efferent side of neural function. In fact, the thoroughness of their exclusion from consciousness suggests that their absence represents a design feature of consciousness providing important clues to its nature and biological function. This in turn helps constrain conceptions of its neural implementation as well as the search for its origin in the phylogeny of life forms.

2. The earthworm’s dilemma and its higher order analogs Earthworms display a swift withdrawal reflex to cutaneous touch (Couteaux, 1934; Darwin, 1883). It is mediated by giant fibers in the segmented worm’s ventral nerve cord. Consider the worm’s initiation of a crawling movement. Such a movement will produce sudden stimulation of numerous cutaneous receptors (‘‘re-afference,’’ von Holst & Mittelstaedt, 1950), yet no withdrawal reflex is released to abort the movement. Apparently the worm’s simple nervous system discounts cutaneous stimulation contingent on self-produced movement as a stimulus for withdrawal. The mechanism for making this functional distinction may be purely peripheral, since both sensory and motor neurons make numerous synapses on the giant fibers involved in triggering withdrawal (Shimizu et al., 1999). Details apart, the net effect is that the lowly worm treats self-produced and other-produced sensory input differentially. It has solved a simple version of a problem that will only grow in magnitude with evolutionary advances in the sophistication of movement and the complexity of sensory systems that guide it. Our own orientation to our surroundings is informed by a rich three-dimensional and multimodal panoramic display we call the world. This spatially extended framework contains a great multiplicity of seen, felt, heard, and otherwise sensed objects. Among these there is one we call our body. It occupies a privileged position in our world by virtue of its perpetual presence as the central object around which the world extends in all directions. This central placement is a result of the means by which we gain access to the world. Our only source of information concerning it is the set of sophisticated sensory arrays and detectors mounted on the surface of and inside our body. Their output is the source of the spatialized panorama we call the world, to which our senses appear to give us direct access. As the taken-for-granted setting for our lives this world is utterly unproblematic: it simply lies there in all its richness as a stable framework for our actions. Yet this appearance is a highly derivative outcome of complex sensory and sensorimotor transformations of the first-order information supplied by our various senses. The problem of the stability of the world is this: The bodily platform on which our sensory arrays are mounted is not only mobile with respect to the world it inhabits, but with respect to itself in the form of complex multijointed movements. The chief exteroceptors are attached to the head of this body, that is, to a body part which in terms of its concatenated degrees of freedom is

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at the farthest remove from the world about which they supply information. This head swivels and translates with respect to the body, and the body in turn supplies multiple sources of translatory and rotatory movement. The visual sense adds the final degree of freedom by allowing its receptor arrays to swivel in sockets within the swivelling head on its flexibly moving body. Virtually every such movement affects the output of the sensors informing us about the world. Even a movement as simple as a single eye movement sets the world sweeping rapidly across the retina in the opposite direction, yet the world we experience undergoes not so much as a tremor on its account. This is the earthworm’s dilemma writ large: information about the world is confounded by selfproduced sensory information derived from movement of the sense-organs. The complexity of such confounding increases with the sophistication of the motor and sensory apparatus involved. The earthworm solved its far simpler problem by discounting sensory afference generated by its own movement. Every advance beyond its level of motor and sensory complexity requires remedies for the contamination of sensory information by self-motion. The result is a variety of mechanisms which either minimize such effects or compensate for them. Examples of the former are provided by the vestibulo-ocular reflex, which counter-rotates the eyes during head movement, and by a variety of global postural adjustment patterns which tend to stabilize the sense organs with respect to the world during movement (Dial, Warrick, & Bundle, 2000; Frost, 1978; Green, 1998; Herbin, Jeanne, Gasc, & Vidal, 2001). Compensatory mechanisms span the gamut from sensory remedies (e.g., saccadic suppression, Matin, 1974; see also Bridgeman, Van der Hejiden, & Velichkovsky, 1994; O’Regan, Deubel, Clark, & Rensink, 2000) to a variety of complex transformations of sensory coordinates between different spatial frames of reference (Gallistel, 1999). They combine information from a given modality with information derived from other systems, chiefly the vestibular, proprioceptive, and motor systems, in order to disentangle sensory information about the world from the information generated by movement of the sense organs themselves (Bell, Bodznick, Montgomery, & Bastian, 1997; Bridgeman, 1983; Colby, 1998; Gauthier, Nommay, & Vercher, 1990; Gr€ usser, 1986; Teuber, 1978; von Holst & Mittelstaedt, 1950; see also Klier, Wang, & Crawford, 2001, and Dean, Porrill, & Stone, 2002). In fact, an entire sensory system—the vestibular—bears witness to the utility for these purposes of accurate information regarding the inertial and gravitational aspects of the position and movements of the head in space (Highstein, 1988). Mechanisms involved in various aspects of remedial measures for sensory effects of self-motion cover the entire length of the neuraxis, from spinal cord, over brainstem, to forebrain. They are richly represented at the cortical level, both in its posterior and frontal regions (Boussaoud & Bremmer, 1999; Colby, 1998), yet our experience gives no hint of their operation. We are aware neither of the problem faced by the spatial senses in this regard, nor of the sophisticated solutions nature has provided as remedies. Our visual world excludes the sudden translation of the world across the retina during the movement of our eyes, and similarly the sum of the sensory effects of all our concatenated multijointed movements: perceptually our world is a stable arena within which we experience ourselves as moving. Apparently consciousness is the beneficiary of the completed operation of all the various compensatory measures. It presents us with only the final result of their smooth conjoint functioning. In the exclusion from consciousness of even a hint of the operations required to synthesize a stable world-space from the activity of mobile sensory systems lies a major clue to the nature of consciousness.

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3. Why we need to be conscious while the earthworm need not be It was noted above that the earthworm, at least in principle, could solve its ‘‘re-afference dilemma’’ by a purely peripheral mechanism. If so, the distinction it makes between self-produced and other-produced sensory afference has no bearing on the issue of consciousness. Presumably its giant fibers trigger withdrawal or not depending on the balance between activation levels of the sensory and motor synapses impinging upon them. If sensory synapses were excitatory on giant fibers, and motor synapses were inhibitory, a workable arrangement might result. There is no obvious reason to invoke consciousness in an account of such a neural mechanism. Nor was it invoked in the above account of the far more complex and sophisticated mechanisms operating to manage the interaction between sensory information and movement in more evolved animals. On the contrary, in perfect agreement with the case of the earthworm, they were portrayed as operating altogether outside the compass of consciousness. Consciousness was invoked, rather, as the domain from which evidence of these neural operations is excluded. Whence then this domain of consciousness from which they are excluded? The evolution of higher animals leads not only to increased complexity of single sensory and motor systems, but produces a diversification of such systems in the equipment of a given species. Vision, hearing, touch, pain, smell, taste, enteroception, proprioception, and vestibular system are some of those on the sensory side, while a great variety of locomotor, orienting, grasping, and manipulatory appendages—often paired, in sets, and with multiple, independently moving joints—proliferate on the motor side. Such diversity brings special problems in its train. On the sensory side, for example, the receptor arrays of different modalities are often disposed quite differently on the body. They are therefore not affected in the same way by self-motion, and so cannot be subject to the same compensatory remedies, nor be integrated directly. On the motor side, different effector organs and their parts may be employed in the service of several—and sometimes conflicting—motivated and goal-directed behaviors: feeding, drinking, grooming, mating, defense, aggression, escape, exploration, and foraging, to name but a few. Such sensory, motor, and behavioral diversity brings with it a rich an intricate set of issues in logistics, control, and resource utilization. These involve multisystem coordination, sharing of and competition for common resources, ranking of behavioral priorities, and decision-making, because behavior, the ultimate outcome of the operation of the many systems, must remain coherent, unitary, and organized (Allport, 1987; Cabanac, 1996; Charnov, 1976; Emlen, 1966; MacArthur & Pianka, 1966; McFarland & Sibly, 1975; Prescott, Redgrave, & Gurney, 1999). Consciousness, it is here proposed, arose as a neural solution to a subdomain of this problem-space, namely as an interface between the spatial senses and the motor requirements of motivated behavior. The setting for this solution is the centralized organization of the brain characteristic of higher animals, including all vertebrates. Not all animals rely on centralized neural organization to control behavior, even when possessed of a brain. A number of invertebrate forms, including insects, concentrate considerable neural resources to segmental ganglia. Their brain is in a sense no more than the anterior-most of these ganglia, in receipt of the output of the specialized receptors of the head. It does not necessarily exercise a command function in the sense of central control of behavior (see Altman & Kien, 1989). This decentralized neural control allows the insect body to survive without its brain.

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Moreover, given adequate somatic stimulation, it will perform many of its behaviors with apparent competence, though naturally without relation to the distal environment (Snodgrass, 1935). A vertebrate, on the other hand, does not survive for more than seconds after the loss of its brain, since in vertebrates even vital functions are under central brain control. The difference with respect to insects is underscored by the contrasting disposition of motor neurons. In insects they are concentrated to segmental ganglia but are rare in the brain (Snodgrass, 1935), while in vertebrates they populate the brain in sets of distinctively organized motor nuclei. Motor control in vertebrates has ‘‘moved up,’’ as it were, to that end of the neuraxis which leads in locomotion and is in receipt of the output of the chief exteroceptors (Grillner, Georgopoulos, & Jordan, 1997). The vertebrate development of a centralized brain plan is as old as the phylum itself, apparently originating with the development of a true neural crest in vertebrate ancestry (Holland & Holland, 1999; Northcutt, 1996). It was presumably driven by the savings achievable by close integration between diverse sources of exteroceptive information and motor control mechanisms for regulating the many behaviors guided by exteroceptive cues. When multiple sources of sensory information are relevant to a diverse range of behaviors, considerations of economy alone argue for sharing of informational and control resources (Prescott et al., 1999). Yet such integration is impeded by the distinctly different ways in which different sense organs are disposed on the body and hence affected by self-motion. Integration between modalities and between them and motor control mechanisms presupposes a resolution of differences between the remedial coordinate transformations and disparate frames of reference in which they are cast (see Gallistel, 1999). The present proposal is that consciousness arose as a comprehensive solution to the logistics problems created by self-motion in one such domain of central control, namely decision processes mediating between motivational, sensory-spatial, and motoric functions in the control of behavior. Such decision processes concern the layout of the surroundings, the presence and position of targets of approach and avoidance within those surroundings, and the many levels and varieties of need possessed by the body whose behavior is being regulated for the purpose of satisfying those needs. Yet between the decision and the target there lies the multidimensional and multiscale flux of motion-produced sensory effects, effects moreover, that differ from one sensory system to another. The solution, it is here proposed, is to make targets available for decision making by presenting them as part of a coherent and stable world-space synthesized from the various concatenated correction measures needed to remove the effects of self-motion from sensory information. On such a basis the spatial senses could be integrated within a common framework serving a number of decision processes. The solution amounts to giving decision mechanisms access to a synthetic ‘‘reality space’’ (cf. Revonsuo, 1995) within which the types of exteroceptive information they require are displayed in a convenient format. More specifically, the evolution of an integrated ‘‘reality space’’ is proposed to have occurred in response to the need, shared by a variety of systems regulating motivated goal-directed behavior, for veridical orientation to the surroundings through the triumvirate of spatial senses: vision, audition, and somesthesis. Decision-mechanisms would benefit from accessing these in a form stripped of the confounding effects of self-produced motion, and the brain would save resources by making the three available in a single unified format which different systems of motivated behavior could share. The result would be an integrated ‘‘world space’’ presenting decision and control mechanisms with a stabilized multimodal synthesis of the distal surroundings in the form

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of a simulated ‘‘real world’’ arena for the control of various goal-directed activities. With potential targets of action presented on such an arena, central decision functions need only decide what to do about them, unencumbered by the compensatory complexities behind the scenes. This arrangement, needless to say, defines the domain of consciousness, according to the present proposal. Such an arrangement introduces the possibility of another great simplification of the tasks of decision functions: once the target is available in a convenient format, decision and control mechanisms can be relieved of involvement in the motor details of target acquisition or avoidance. Generally speaking we are not aware of the intricate complexities of motor control required to activate and coordinate the multitude of musculoskeletal adjustments involved in translating our intentions into behavior. Once an intention to act has arisen and a target for action has been selected, the execution of, say, a reaching movement takes place with smooth automaticity. We are not conscious of the orchestration of the many muscle contractions and feedback adjustments which that multijointed movement in fact involves (Bernstein, 1967). Like the sensory transformations already considered, extensive neural resources are devoted to these motor requirements, from high cortical to spinal levels, yet we are spared awareness of their operation at the level of consciousness. The reason is the same as before: once the target is presented in the appropriate format, decision mechanisms can confine their resources to the level of goals and intentions, and leave the details of motor execution to routine mechanisms beyond their purview. Accordingly, a number of the spatial frames of reference into which sensory information is mapped in the brain are cast in action-oriented data formats (Colby, 1998; Sparks, 1988). There are, in other words, multiple functional considerations which converge on the potential utility of introducing a ‘‘reality space’’ arrangement as part of the control economy of a centralized brain plan. The most obvious candidate for such a neural system in the vertebrate brain is the multimodal laminar structure crowning the upper brainstem, namely the tectum in the roof of the midbrain. Its fundamental organizational theme is multisystem convergence from many parts of the brain onto a laminar scheme for topographic integration of the principal spatial modalities within a common efferent framework (Bartels, M€ unz, & Claas, 1990; Bastian, 1982; Edwards, 1980; Grobstein, 1988; Gruberg & Harris, 1981; Harting, Updyke, & Van Lieshout, 1992; Ingle, 1973; Knudsen, 1982; Nemec, Altman, Marhold, Burda, & Oelschl€ager, 2001; Niemi-Junkola & Westby, 2000; Schiller & Lee, 1994; Smeets, Nieuwenhuys, & Roberts, 1983; Stein & Meredith, 1993; Wallace, Wilkinson, & Stein, 1996). Diverse tectal afferents give numerous specialized systems—including motivational ones (Ewert, 1987; Telford, Wang, & Redgrave, 1996)—access to its integrated multimodal mapping of body and surrounding space (Scheibel & Scheibel, 1977). Within this structure, vestibular (Bartels et al., 1990; Frens, Suzuki, Scherberger, Hepp, & Henn, 1998), and eye-position information (Groh & Sparks, 1996; Knox & Donaldson, 1995; Sparks, 1988; Van Opstal, Hepp, Suzuki, & Henn, 1995) may perform essential intermodal registry and stabilizing functions, while competitive interactions accomplish target selection (Grobstein, 1988, p. 45; Horowitz & Newsome, 1999; Niemi-Junkola & Westby, 2000; Ratcliff, Segraves, & Cherian, 2001; Wurtz & Mohler, 1974). In some non-mammalian vertebrates this structural complex forms the single largest compartment of the brain as a whole, as illustrated schematically in Fig. 1. We cannot easily ask these lower vertebrates whether in fact they are conscious, that is, whether they see the targets to which their behavior relates, but if they do, there can be little doubt that it is the neural apparatus housed in the multimodal and laminar topographies of their bulging tecta which

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Fig. 1. Outline of the brain of the zebrafish, a small tropical teleost fish, to illustrate the proportions of externally visible brain compartments in a lower vertebrate. Side view is shown below, outline of a cross section from the approximate level indicated by the dashed line is shown above. Abbreviations: C, cerebellum (partly hidden); H, hypothalamus; Tel, telencephalon; TO, optic tectum, or roof of the midbrain. Shaded triangle in lower part of the figure indicates the approximate extent of territories included under the concept ‘‘core control system of the upper brainstem’’ in Section 5 of the text. After Wullimann, Rupp, and Reichert (1996).

allows them to do so. This issue will be given further consideration in connection with the complexities added by mammals to be discussed in Section 5, below. To summarize the foregoing: the logistic problems attendant on the sensory orientation needs of complex, moving, and multijointed bodies led to a division of labor in the evolution of centralized brains between a domain devoted to environmental guidance of goal-directed behavior on the one hand, and domains devoted to the sensory preliminaries and motor sequels of central control functions on the other. Primitive animals make do with local, piece-meal solutions, while higher animals have opted for a comprehensive solution reflected in the central organization of their brains. As part of that central organization they are proposed to have evolved a neural arrangement in which central decision making is supplied with the end-product, rather than the movement-contaminated preliminaries, of sensory afference. It takes the form of a synthetic, stabilized, and coherent neural simulation of the animal’s body in relation to its surrounding space. This in turn enables motivated behavior, via appropriately structured motor mechanisms, to be controlled at the level of goals, targets, and intentions rather than at the level of motor detail.

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An elegant way to structure such an arrangement would be to embed a central representation of the body, whose movements and other actions are to be controlled, within a central representation of the world, with respect to which that body is to be controlled, and to embed decision making processes within the representation of the body whose movements they control. This amounts to a nested, tripartite, arrangement of the ‘‘reality space.’’ Two of its domains, namely world and body, are spatialized and object-like, while the third is a domain of decision-making. The latter enters consciousness only in the form of a sense of motivated agency, that is, without being represented in spatialized, object-like fashion as are the other two domains. It might be designated ‘‘the self’’ for convenience. It is the central claim of the present paper that such an arrangement actually emerged in the course of the evolution of centralized brains, and that our own conscious experience of our world, body and self is nothing other than the actual on-line working of a neural embodiment of such an arrangement. The world with its myriad objects and events coherently deployed in space, the body which interacts with that world from its central location within it, and the sense of motivated agency which inheres in that body would, accordingly, be the functional content of this nested neural arrangement. A highly schematic illustration of the elements of this conception, in Venn diagram form, is provided in Fig. 2. Note that the disposition of the diagram provides interfaces between sensory and motor, sensory and motivational, and motivational and

Fig. 2. Highly schematic and abstract depiction of the conception of a neural ‘‘reality space’’ as a subdomain of brain function, in Venn diagram form. The brain as a whole is represented as a circle, within which subdomains demarcate functional compartments. The conscious domain of the tripartite synthetic ‘‘reality space’’ is left unshaded. The heavy line separating the reality space from other domains indicates the exclusion of those domains from consciousness. Arrows mark interfaces across which information may pass without entering consciousness.

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motor domains separate from and independent of the domain of consciousness. These interfaces provide scope for a variety of priming, implicit, and unconscious phenomena to affect behavior without entering consciousness.

4. The testimony of conscious contents Consciousness is ‘‘located,’’ in other words, at the end of or after the processes through which the image of a stable world is extracted from moving sensory arrays, but before or prior to the processes through which intentions are unpacked into the details of musculoskeletal control. As such it would seem ideally placed to contribute to the decision- and control processes that give to behavior its unitary and integrated character (Allport, 1987; Cabanac, 1996; McFarland & Sibly, 1975). Stripped of the complex transformations needed to synthesize a stable world from mobile sensors and unencumbered by the details of motor execution, consciousness provides a summary display of an individual’s current situation well suited for on-line optimization of behavioral priorities from moment to moment. Thus, for example, this summary display cannot dispense with the high degree of perceptual detail available to consciousness since that level of detail on occasion turns out to be crucial for determining behavioral priorities, as when one notices that one of the bars of a cage housing a starved and ferocious carnivore happens to be traversed by a hairline fracture. The above construal of the nature of consciousness is supported not only by the two major exclusions from consciousness already reviewed, namely sensory preliminaries and motor sequels, but by the fact that a major category of information bearing directly on decision-making is included within its compass, namely the vast array of emotional/motivational biassing variables experienced as feelings, affects, moods, and sentiments. These biassing variables span the range from physical pain over phenomena such as, joy, fear, hunger, anger, grief, and sexual desire to the attractiveness of the smell of fruity esters, the nagging feeling that there is something wrong with a certain argument, and a sense of sublimity. They include all the ways in which the meaning, significance as well as hedonic quality of objects or circumstances enter experience, whether on an innate or acquired basis. Though these biassing variables are truly diverse in their origins and mechanisms they all have two things in common: they bear on behavioral decisions and they do enter consciousness (cf. Cabanac, 1996). Particularly revealing in this regard are functions which straddle the fence between unconscious and conscious processes, such as those involved in the control of respiration. Under normal circumstances the adjustment of respiratory rate and tidal volume needed to keep blood gases within normal bounds is automatic, effortless, and unconscious. Should, however, the partial pressures of blood gases go out of bounds that fact intrudes most forcefully on consciousness in the form of an acute sense of panic. Why? Such a situation generally means that routine respiratory control no longer suffices but must be supplemented by an urgent behavioral intervention of some kind. There may be a need to manually remove an obstruction covering the airways or to get out of a carbon-dioxide filled pit. Such measures ought momentarily to take precedence over all other concerns. It is at that point, when crucial action on the environment is of the essence, that blood gas titres ‘‘enter consciousness’’ in the form of an over-powering feeling. Physiological functions which never are subject to ‘‘remedial action,’’ on the other hand, such as

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accommodation of the eye’s lens to different target distances, are not represented in consciousness even when driven, as in this case, by exteroceptive information. Another example will help define further the functional role of consciousness as a modality serving decision processes, in this case affecting prospective deliberate planning. Reflex withdrawal of a limb occasioned by noxious stimulation precedes awareness of the pain, or at least is too fast to allow conscious guidance to have much influence over the act of withdrawal itself. Yet the pain forcefully enters consciousness nevertheless. As in the previous example, preparedness for more elaborate remedial action than reflex withdrawal may help explain this fact. An additional reason is supplied by the utility of experienced pain for revising the informational base utilized in the deliberate planning of future behavior. Informally speaking pain signals a condition whose continuation would lead to death. The situations in which it has been experienced accordingly deserve high priority when it comes to planning behavior, and ought therefore to be remembered. The type of memory available to conscious access for deliberate planning is declarative memory, which requires awareness/attention for its storage (see Druckman & Bjork, 1992 and Shanks & St. John, 1994). In order for an experience involving noxious stimulation to affect future decision-priorities involved in the conscious guidance of behavior the pain must enter consciousness and thereby leave a trace in declarative memory. This makes it part of the mnemonic informational base that allows central decision functions to plan future behavior appropriately. The many bodily scars and injuries accumulated by those rare individuals who are born without a sense of pain presumably reflect, at least in part, the absence of the cautionary effect on deliberate planning normally produced by the memory of past pain. Consciousness appears to supply a specific forum for the on-line integration of the functionally highly diverse kinds of information represented by environmental information, motivational state, and memory of past experience jointly bearing on decisions regarding ‘‘what to do next,’’ presumably via the type of capacity-limited competitive selection that has figured in models of central decision processes since the time of Broadbent. This would mean that conceptions of the function of consciousness that link it primarily to capacity limitations of, say, selective attention or working memory (see Baddeley, 1993; Mandler, 1975; Posner & Rothbart, 1991) and those that identify it with decision- and action-related control functions (see Allport, 1987; Hilgard, 1992; Norman & Shallice, 1986) concern the same central function (see further Section 5, below). Its task is to optimize behavior from moment to moment in light of its diverse contents. To do so, it cannot be implemented at the level of any of its contributing sources of information, such as a mechanism for, say, deliberate effort dependent on dorsolateral frontal cortex, since the capacity of such a mechanism to control behavior competes with others, such as those mediating fear, hunger or intrusive novelty. In competition with sufficient levels of such information deliberate effort often proves impotent, indeed. Competitive interactions whose outcomes in fact gain control over behavior are likely to involve highly convergent interfaces of multiple neural systems in the upper brainstem (Swanson, 2000; see further next section). If consciousness bears this intimate relationship to decision and control functions involved in optimizing behavioral choices in the light of diverse types of information, it is directly involved in the fate and survival of the body and brain in which it is housed. It helps steer, as it were, the behavior of a physical body in a physical world, to neither of which it has any direct access whatsoever. What it does have direct access to—this being the very point of the arrange-

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ment—is the neurally simulated body and world of the ‘‘reality space’’ on the basis of which it determines ‘‘what is up, and what to do next.’’ We call that neural body and that neural world our body and our world. A further reason now becomes apparent for the necessity to exclude from consciousness any sign of the transformations through which the stable panorama of the world is derived from the sense organs: the rich ‘‘reality space’’ of consciousness, crowded with objects and events, must be taken to be absolutely real, or the entire motivational underpinnings of behavior collapse. The credibility of that reality is a good reason not to let the trappings behind its surface show through, because life depends on taking its appearances seriously. Hints about the importance of this matter are available in the disorienting effects that may attend a breakdown of the exclusion mechanisms which normally present us with a familiar and stable world. Some, but far from all, experiential effects of a variety of abnormal conditions spanning from mental illness over sensory deprivation, extreme sleep deprivation, emergency levels of arousal, and hypnagogic imagery to drug-induced hallucinosis are interpretable in this light. When a subject under the influence of a hallucinogen experiences that a head movement leads to wholesale wobbling of the world, the most parsimonious interpretation is that the gain of a visual-vestibular compensatory mechanism has been altered. The lack of full compensation suddenly intrudes on consciousness in the form of movement of the world, and this may alert the subject to an epistemic connection normally hidden from awareness. Dramatic alterations in the normal arrangement of the ‘‘reality space’’ of consciousness may be triggered not only by drugs, but by direct stimulation of the human brain (Blanke, Ortigue, Landis, & Seek, 2002). It lies beyond the scope of this paper to explore potential clinical implications of the present perspective. Suffice it to note that they do exist. They point to the crucial role in all aspects of normal, waking adaptation of the ‘‘exclusion mechanisms’’ through which consciousness presents us with a synthetic and orderly ‘‘reality space.’’ In as far as it is clinically normal waking consciousness and making allowance for marginal exceptions such as perceptual illusions, it is the only dependable reality to which we have access. Barring the kinds of phenomena just referred to, which are only altered or deranged ‘‘reality space’’ phenomena, we have nothing to compare it with, so it constitutes our ‘‘real reality’’ by default, as it were. Nor is there any reason to mourn this fact. The honing action of natural selection and the tuning action of learning mechanisms have ensured that it provides a reflection of circumstances in the physical universe eminently capable of serving the orientation needs of complex, mobile animals. The defining trait of consciousness is, in other words, not any special ‘‘feel’’ or other hypothetical qualitative marker of consciousness, but the simple fact of finding oneself in a world—any world— and ultimately, stripped to its minimal essentials, to be in the presence of any object whatsoever (for details, see Merker, 1997). Nor is there, in principle, any particular level of complexity required of the world or object supplying the content of the conscious state: we can subtract one modality and channel capacity after another without for that reason altering the fact of consciousness itself. In practice, however, the scenario for the origin of the ‘‘reality space’’ arrangement presented here suggests that such an arrangement is likely to arise only with the attainment by mobile animals of a certain level of sensory system diversity and motor sophistication on the basis of a centrally organized brain plan. This in turn suggests ways of posing questions related to anatomical arrangements and the phylogenetic distribution of consciousness in animal forms.

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5. The core control system of the upper brainstem Already the earthworm faces some aspects of the contamination of sensory input by selfproduced movement, but its problem is soluble, at least in principle, by a peripheral mechanism which relieves it of any necessity to be conscious. The latter function, rather, was proposed as a measure of neural resource economy in animals whose diversity and sophistication of sensory and effector systems is such as to benefit from coordination and control through the integration of spatial modalities and decision processes within a centrally organized nervous system. More specifically, the utility of a unitary and movement-stabilized ‘‘reality space’’ synthesized from the chief spatial senses to supply the orientation needs of a variety of goal-directed (motivated) behaviors was proposed as the key to the evolution of consciousness. Brief mention was made of the roof of the midbrain as a candidate brain site whose characteristics lend themselves to the implementation of such a ‘‘reality arena’’ mechanism. Needless to say, anatomical commitments of this kind are a separate matter from the rationale which leads one to look for an implementation scheme. Such commitments must as yet be provisional and tentative. Yet it might nevertheless be of interest to ask how the suggestion based on highly conserved features of the vertebrate brainstem might be related to the complexities that arise with elaboration of the forebrain, and of the thalamocortical complex in particular, in mammals. One advantage of doing so is that it allows us to bring human first hand evidence regarding consciousness to bear on the issue. At first sight such a confrontation augurs ill for the suggestion made in Section 3. When a zebrafish darts about gathering specks of food in its aquatic environment, it presumably relies on the neural machinery housed in its bulging tectum, depicted in Fig. 1. We cannot ask it if it sees the specks to which it orients with such competence, but we can ask humans whose cortical visual system has been damaged whether they see stimuli presented in the affected parts of their visual fields. They are capable of pointing with reasonable competence to stimuli appearing in visual field locations corresponding to the cortical damage (see review by Stoerig & Cowey, 1997). The phenomenon is infelicitously named ‘‘blindsight,’’ because to a first approximation patients do not see these stimuli to which they point when pressed to guess their locations. Since the roof of their midbrain has not been damaged, it appears that the tectal machinery by itself is not sufficient to sustain visual awareness in these patients. We might accordingly conclude that the zebrafish also does not see the stimuli to which its tectum orients it with such alacrity. But that conclusion overlooks a number of complications which might make it premature. First of all, the responses are only superficially similar. The zebrafish orients spontaneously to the stimuli in question, while the patients never do. They must be cajoled to even try, and sometimes they do so over voluble vocal protests. To bear on the tectal issue, subject reports must deny awareness of stimuli to which spontaneous orienting movements are directed, which is quite a different matter. Moreover, in view of the direct cortical projection to the roof of the midbrain (Harting et al., 1992), it cannot be assumed that the tectal machinery is functionally intact following cortical damage. Its functional integrity may be dependent on the massive—and symmetrical—cortical input it normally receives in mammals, not only directly, but indirectly, via the substantia nigra (Wallace, Rosenquist, & Sprague, 1989). The close interdependence of cortical and collicular mechanisms in this regard is demonstrated most strikingly by the fact that the hemianopic blindness induced by unilateral removal of cortical visual areas in cats (or the neglect produced by more restricted interventions)

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recovers on sectioning of the intercollicular commissure or otherwise restoring functional symmetry by inactivating additional structures (Kapur, 1996; Lomber & Payne, 1996; Lomber & Payne, 2001; P€ oppel & Richards, 1974; Sprague, 1966; Wallace et al., 1989). The expectation that in such a case collicular lesions by themselves should have the same dramatic effect as the cortical damage is confounded by the fact that the cortical visual system has access to the brainstem motor system independently of the superior colliculi (Schiller, 1977; Tehovnik, Lee, & Schiller, 1994). The visual performance made possible by extra-collicular connections in an animal with collicular damage cannot as a matter of course be assumed to be conscious, since performance may be dissociated from consciousness. The ‘‘blindsight’’ phenomenon is not alone in showing this. In certain forms of epilepsy behavioral sequences of considerable complexity (such as speech) may be performed without awareness. In fact, Penfield and Jasper (1954) concluded that the complex nature of some epileptic behavior implies cortical mediation. This in turn helped them conclude that the system responsible for consciousness must be subcortical (‘‘centrencephalic,’’ a conception to which we shall return). Cases of human collicular damage are rare, but in one such case whose damage extended into the midbrain tegmentum (Denny-Brown, 1962) the symptoms were severe, consisting of profound apathy with ‘‘no evidence of recognition of people or of any event in her surroundings.’’ This points to the potential importance of the extent of midbrain damage in determining outcomes—a point also underscored by the findings on macaques in the same report—and to the significance of spontaneous, self-initiated behavior and reactivity in this regard (cf. Dehaene & Naccache, 2001). Finally, it should be noted that cortically blind patients who deny ‘‘seeing’’ in their blind field may still be vaguely aware that ‘‘something’’ is taking place within its confines in the testing situation (Singer, Zihl, & P€ oppel, 1977, p. 188; Stoerig & Cowey, 1997, patient G.Y., p. 555). Such bare awareness of ‘‘something’’ may not impress those accustomed to seeing the world as we normally do. It may not even qualify as visual awareness (see, however, Stoerig & Barth, 2001), yet it is awareness nevertheless. If such awareness is mediated by subcortical mechanisms (which need not be the case in ‘‘blindsight’’ since non-primary visual cortical areas are spared. See Sahraie et al., 1997) they would have to be credited with the capacity to implement the fundamental function of consciousness: bare awareness of ‘‘something.’’ To summarize, the fact that cortical information enters consciousness does not by itself tell us where it does so, nor how the system needed for it to do so is organized. Till the many issues referred to above are resolved empirically it may be useful to try to delimit the scope of corticalsubcortical interactions potentially involved in the organization of consciousness. The ‘‘realityspace’’ conception of the organization of the vertebrate upper brainstem alluded to in Section 3 above may provide a point of departure in this regard: how is it related to the drastically expanded thalamocortical complex of mammals? (Please note that in what follows the dorsal thalamus, because of its overwhelmingly rostral, corticipetal, efference, is treated as a cortical dependency whose functional role is entirely internal to the thalamocortical complex. Its internal organization bearing on consciousness will not be considered here, but see, e.g., Newman, Baars, & Cho, 1997). In fact, cortical efference to this upper brainstem region is massive. It issues from cortical areas of every description, rather than from those of motoric specialization only (Harting et al., 1992; Kuypers & Lawrence, 1967). Through these projections cortical information is added or ‘‘grafted’’ onto a highly conserved system of vertebrate environmental guidance and decision-making. It enters that pre-existing anatomy along what, for present purposes, may be described as three

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highly convergent ‘‘projection funnels:’’ the direct cortico-hypothalamic projections (Swanson, 2000), the cortico-striato-pallido-nigral projections (Swanson, 2000), and the direct cortico-collicular projections (Harting et al., 1992; Kuypers & Lawrence, 1967). Each of these originates in numerous cortical areas with diverse specializations, areas which cover vast, but not entirely identical, cortical expanses (see Fig. 3). Their target areas jointly define what might be called the ‘‘core control system of the upper brainstem.’’ Its cell territories in turn issue direct efferent projections to pre-motor and motor structures of brainstem and spinal cord. They are also intricately interconnected with one another as well as with various parts of the forebrain, cortex included. In addition to hypothalamus, substantia nigra, and superior colliculus this core control system includes the ventral tegmental area, the midbrain reticular formation, the zona incerta, the red nucleus, the periaqueductal grey matter, and a set of nuclei in the isthmic transition region from midbrain to pons, namely nucleus cuneiformis, pedunculopontine and laterodorsal tegmental nuclei, locus coeruleus and the rostral raph
e complex.

Fig. 3. Highly schematic depiction of essential anatomical elements of the ‘‘core control system of the upper brainstem’’ described in Section 5 of the text. Parasaggital side view is shown below, and a crossection in the approximate plane marked by oblique arrows is shown above. Cellular territories included in the ‘‘core control system’’ are marked by oblique shading, except for the zona incerta (V) which is left unshaded for the sake of clarity. The separately marked caudal shaded territory represents the mesopontine ‘‘state control’’ nuclei. Systems described in the text are identified by the symbol marking sites of origin of their afferents and/or efferents. Open squares, the direct cortico-collicular projection ‘‘funnel’’ with a posterior cortex bias. Open triangles, the direct cortico-hypothalamic projection ‘‘funnel’’ with a frontal cortex bias. Open circles, the cortico-striato-pallido-nigral projection ‘‘funnel,’’ also with a frontal bias (though not identical to the cortico-hypothalamic one). Filled squares, finally, mark a small sample of zona incerta connective relations. Incertal cortical afference is dominated by but not restricted to the cingulate gyrus (indicated here by its location inside the dotted line demarcating ‘‘limbic’’ components of the telencephalon). Abbreviations: D, dorsal thalamus (dotted line encloses midline and intralaminar nuclei); V, ventral thalamus (zona incerta ventrally, thalamic reticular nucleus dorsally); H, hypothalamus; g, medial geniculate body (caudal extreme); lh, lateral hypothalamus; m, mammillary bodies; mrf, mesencephalic reticular formation; p, periaqueductal grey matter; r, red nucleus; sc, superior colliculus; sn, substantia nigra.

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This continuous crescent of cellular territories extending from colliculus to hypothalamus houses structures each of which performs functions in some way linked to essential aspects of consciousness or its contents discussed in the foregoing. Its mesopontine nuclei together with the midbrain reticular formation are pivotal structures determining global behavioral state through the serotonergic, adrenergic, and cholinergic systems regulating sleep cycles, wakefulness, activity levels, and vigilance. They set the ‘‘boundary conditions’’ for consciousness, as it were. The hypothalamic cell groups with their pituitary appendage form a compact nuclear complex integrating endocrine regulation, visceral control, and motivated behavior (Swanson, 2000). Together with the periaqueductal grey matter (Panksepp, 1998) they presumably supply a good part of the hedonic and emotional content of consciousness. The remainder of the core control structures are involved in the selection, decision, and up-dating functions ensuring the coherence of behavior and its integration with the layout of the environment: the caudal outposts of the hypothalamus, the mammillary bodies, appear to be part of a dead reckoning system (based on head direction) for locomotor navigation of the environment (Swanson, 2000; Taube, 1998). It presumably acts in concert with the ‘‘midbrain locomotor region’’ associated with the nucleus cuneiformis (Grillner et al., 1997; Shik, Severin, & Orlovskii, 1966). The colliculus itself, as already mentioned, crowns this control system with a laminar scaffolding containing a body map integrated with topographic mappings of visual and auditory space. It receives projections from widespread areas of neocortex, and—significantly—integrates both streams of the cortical visual system. The cortical projection to the midbrain roof ignores collicular boundaries to continue into the periaqueductal gray matter ventromedially (Harting et al., 1992) and into midbrain reticular territories ventrally (Kuypers & Lawrence, 1967). In control terms, the collicular system complements the locomotor navigation system with phasic behavioral adjustments to environmental contingencies epitomized in (but not limited to) the orienting reflex (see Dean, Redgrave, & Westby, 1989; Dean & Redgrave, 1984; Masino, 1992; Merker, 1980; Schneider, 1969; Telford et al., 1996; Werner, Dannenberg, & Hoffmann, 1997). The ventral tegmental–nigral component, finally, expresses the outcome of basal ganglia selection and queuing of behavioral priorities at the midbrain level. Staggered competitive elimination of alternatives along the progressively narrowing cortico-striato-pallido-nigral funnel is translated into behavior via a massive and tonically inhibitory nigral projection to the colliculus, among other targets (cf. Gurney, Prescott, & Redgrave, 2001a, 2001b; Prescott et al., 1999). A sophisticated control system needs some means for resolving residual conflict among alternatives left unsettled by routine mechanisms because of stochastic happenstance in a complex multicomponent system or because of exceptional combinations of contingencies encountered in a lively and unpredictable world (e.g., simultaneous and equally attractive but incompatible choices). Such a monitoring function may be performed by the anterior cingulate at the cortical level (Botvinick, Braver, Barch, Carter, & Cohen, 2001; Bush, Luu, & Posner, 2000; MacDonald, Cohen, Stenger, & Carter, 2000). At the level of the core control system the zona incerta—whose most prominent source of cortical afference is the cingulate cortex (Mitrofanis & Mikuletic, 1999, Figs. 6, 7)—seems optimally placed to play such a role. This sizeable wedge of cells interposed between the lateral hypothalamus and the dorsal thalamus is—along with the thalamic reticular nucleus and the ventral lateral geniculate nucleus—an embryological derivative of the thalamus ventralis, a basic subdivision of the vertebrate diencephalon (Kuhlenbeck, 1948). The thalamus ventralis of non-mammals receives diverse multisystem afference not only from all parts of the

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telencephalon including the striatum, but from epithalamus, dorsal thalamus, and hypothalamus as well as from the midbrain tectum (Heier, 1948; Herrick, 1933; see also Nieuwenhuis, Ten Donkelaar, & Nicholson, 1998). Its efferents are largely directed caudally, into the medial longitudinal fasciculus, but also into the hypothalamus. In mammals it is the zona incerta among ventral thalamic derivatives which retains this connectional signature of profuse and diverse afference (Kolmac, Power, & Mitrofanis, 1998; Mitrofanis & Mikuletic, 1999; Roger & Cadusseau, 1985; Shammah-Lagnado, Negrao, & Ricardo, 1985), while adding an impressive diversity of efferents (Kolmac et al., 1998; Ricardo, 1981; Romanowski, Mitchell, & Crossman, 1985). These include not only a topographically organized projection to the intermediate and deep layers of the superior colliculus (Kolmac et al., 1998; May, Sun, & Hal, 1997), but a peculiar pattern of contralateral projections to the midline, intralaminar, and association nuclei of the dorsal thalamus as well as to the opposite zona incerta itself, tying these together across the midline (Power & Mitrofanis, 2001). Add to this an internal system of global and mutual connectivity between its four major subdivision (Power & Mitrofanis, 1999), each of which is histochemically distinct (Kolmac & Mitrofanis, 1999) with distinct external connectivities (Power, Kolmac, & Mitrofanis, 1999; Romanowski et al., 1985), and the zona incerta emerges as a unique structural complex highly suggestive of a role in superordinate control functions of potential relevance for mechanisms of consciousness. Let it therefore be suggested here, speculatively and tentatively, that the profuse and unusual connectivity of the zona incerta (or thalamus ventralis of non-mammals) allows it to perform the vertebrate brain’s final conflict monitoring function, and that its internal global self-connectivity (likely to feature substantial GABAergic inhibitory interactions, see, e.g., Bartho, Freund, & Acsady, 2002; Nicolelis, Chapin, & Lin, 1992; Shaw, Simpson, & Lin, 2001; Taylor & Perney, 2001) serves to resolve whatever residual decision conflicts are left unresolved by other mechanisms. The fact that the four principal incertal subdivisions differ in histochemistry and external connections yet are all mutually interconnected with one another (Power & Mitrofanis, 1999) would seem to impose a curious four-partite ‘‘channel’’ structure on decisions taking place via that internal connectivity. The function of such an arrangement is obscure, lest it bear on the apparently general informational limitation of capacity to four concurrent items (Cowan, 2001), a type of limit which yields similar estimates in subjects as different as rat and human when assessed by comparable methods (Glassman, Garvey, Elkins, Kasal, & Couillard, 1994). Be that as it may, the outcome of the interaction between numerous incertal afferents via mutual connectivity linking the incertal subnuclei would be superposed as a biassing signal on the activity pattern of the many and diverse structures that receive zona incerta projections (many of which reciprocate the incertal projection: Kolmac et al., 1998; Power et al., 1999). Notice that the loss of such a function need not produce conspicuous behavioral symptoms. Since it deals preferentially with residual decision making, routine functions may run smoothly in its absence (cf. cingulotomy: Teuber, Corkin, & Twitchell, 1977). Yet as a component of a mechanism of consciousness, such a function is likely to assume a peculiar status in the subjective life of a conscious being. As the final arbiter, by competitive interaction ‘‘within itself,’’ as it were, of conflicts not otherwise resolved, it may well be experienced as a nodal point of ‘‘active agency’’ within consciousness, thereby promoting an incipient sense of ‘‘unconstrained choice’’ or ‘‘free will.’’ Moreover, as a centrally connected monitor function it may supply consciousness with that subjective presence of a tacit ‘‘witness’’ to its contents which is at the

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heart of the very concept of consciousness (see Merker, 1997). These characteristics would amount, in other words, to a subjective sense of self, not in the sense of a self-image—which is a content of consciousness—but in the sense of the nodal monitoring function presupposed by all contents of consciousness. It would be that ‘‘for which’’ these contents are present as seen, felt, and heard objects, a role essential for the ‘‘unity of consciousness.’’ It was called the ‘‘synthetic unity of apperception’’ by Kant, the ‘‘pure subject of knowing’’ by Schopenhauer, the saksin (‘‘witness’’) in Vedanta philosophy, and the ‘‘seeing’’ as opposed to ‘‘seen’’ part of the totality of consciousness in the Alayavijnana doctrine of Mahayana Buddhism (see Merker, 1997, and references therein). If indeed this subtle and often tacit functional component of consciousness is an expression of the role of the zona incerta in the control economy of the mammalian brain, it is of interest that the prime brain site for the induction of generalized epileptic seizures by carbachol (a cholinergic agonist) is the zona incerta (Brudzynski, Cruichshank, & McLachlan, 1995; Cruickshank, Brudzynski, & McLachlan, 1994; see also Hamani, Sakabe, Bortolotto, Cavalheiro, & Mello, 1994). When Penfield and Jasper (1954) formulated their hypothesis of a subcortical ‘‘centrencephalic system’’ responsible for the highest integrative (conscious) functions of the brain, one of their reasons was that the ‘‘absence seizures’’ of epilepsy seemed ‘‘generalized from the start,’’ and specifically compromized the highest, conscious, functions of the brain’s operations. They conceived this system to be centered on the core of the diencephalon and midbrain. It was never specifically delimited in anatomical terms, though the potential role of the midline and intralaminar nuclei of the dorsal thalamus was emphasized (see Bogen, 1995). This emphasis may have been premature, or too specific. The symptoms of intralaminar lesions caused by bilateral paramedian thalamic infarcts are those of a disorder of global regulation of behavioral state, such as coma (often quite transient), torpor, and somnolence, rather than those of a specific affliction of consciousness (Gentilini, De Renzi, & Crisi, 1987; Graff-Radford, Tranel, Van Hoesen, & Brandt, 1990; Guberman & Stuss, 1983; see also Schiff & Plum, 2000). Somnolent patients of this type are conscious during the (shortened) periods of wakefulness they experience. Eventually they may recover to the point of leading relatively normal lives, though their intralaminar nuclei are compromized. Spells of absence epilepsy, on the other hand, compromize consciousness specifically without inducing sleep or coma (Stefan & Snead, 1997). The zona incerta is directly connected with key upper brainstem structures implicated in various aspects of the physiology of generalized seizures: substantia nigra (Deransart, Le-Pham, Hirsch, Marescaux, & Depaulis, 2001), dorsal midbrain (Shehab, Simkins, Dean, & Redgrave, 1995), and thalamus (Danober, Deransart, Depaulis, Vergnes, & Marescaux, 1998, & references therein; Seidenbecher & Pape, 2001). Its central position in this context is particularly noteworthy in view of its prominent contralateral projection to thalamic intralaminar and association nuclei as well as to itself. These projections across the midline may be involved in the generalization of seizure activity, helping to explain the stimulation results of Velasco et al. (1997). Taken together this indirect evidence suggests a potential role for the zona incerta in mechanisms promoting the generalized seizures of absence epilepsy. Should absence seizures turn out to be linked to zona incerta malfunction or mediation, this would add strength not only to the Penfield and Jasper ‘‘centrencephalic’’ hypothesis of consciousness, but to the specific form of it suggested here, and summarized in Fig. 3.

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6. Implications for the phylogeny of consciousness The foregoing may be summarized as follows: The upper brainstem of vertebrates houses a set of structures suggestive of forming a control system for the environmental guidance of motivated behavior and decision making. This system is crowned by the laminar superposition of the chief spatial senses in the roof of the midbrain. Movement-related signals known to be present in this laminar structure may effect inter-modal registry and stabilizing functions for the synthetis of a global ‘‘reality space’’ serving target and goal related decision and control functions. In addition to a spatial body map embedded in visual–auditory space in the layers of the tectum–colliculus, the core control system includes a set of mesopontine nuclei regulating global state, a hypothalamic-periaqueductal system of motivational drive and emotional expression, a nigral system conveying striatally-derived action priorities, and a zona incerta as a central monitor (‘‘self’’) resolving residual resource conflicts. These structures together are proposed to form the essential scaffolding of the mechanism of consciousness in vertebrates. They are contained, by and large, in the central sector of the vertebrate neuraxis marked by a shaded triangle in the lower part of Fig. 1. The new and sophisticated informational resources that become available to mammals with the elaboration of their thalamacortical complex are conceived to supplement rather than to displace this pre-existing brainstem system by supplying its highly conserved structures with a new level of informational content, drawing heavily on long-term integration of individual experience (see Merker, 2004). The zona incerta, through its close connective relations with both the thalamocortical complex and the core control system, ‘‘straddling’’ the two, as it were, would seem ideally placed to play a key role in the kind of interactions between the thalamocortical complex and the core control system that in mammals constitute consciousness. In lower vertebrates, lacking these elaborate interactions, the presence of a stabilized ‘‘reality space’’ in the roof of the midbrain in conjunction with the convergent connectivity of their ventral thalamus may sustain a form of less elaborate consciousness. Even if limited—in some forms—to a bare awareness of the presence of ‘‘something’’ in a location related to body orientation, this would amount to the possession of consciousness of a kind that might result from the selection pressure outlined in the foregoing. If so, what might this tell us about the existence of consciousness beyond the bounds of vertebrate phylogeny? Are there conscious animals without a vertebral column? The perspective just applied to vertebrates immediately suggests candidates for consciousness among the large-brained molluscs: cephalopods such as octopus and cuttlefish. They have welldeveloped multiple sensory systems (Williamson, 1995) which besides mobile eyes and vestibular systems comparable to those of vertebrates include a lateral line system (Budelmann, 2000; Budelmann & Young, 1993). Squid possess specialized neck proprioceptors monitoring headto-body position (Preuss & Budelmann, 1995). Cephalopods have a considerable behavioral repertoire (Hanlon & Messenger, 1996), and their nervous systems have been centralized at least to the extent of bridging the greatly enlarged anterior ganglia of the dual mollusc nerve cord with neural lobe tissue (Young, 1971; see also Budelmann, 1994, 1995). This presents a situation in some respects comparable to that for lower vertebrates just considered. It is not clear, however, to what extent truly central integration of multiple sense modalities is present in cephalopod brains, and little is known about the extent to which cephalopods have a ‘‘body sense’’ based on centrally

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projecting touch receptors or muscle proprioceptors. From the present perspective the issue of consciousness in cephalopods therefore hinges on a clarification of these issues, and ultimately on determining whether their brains are organized in such a manner as to give central decision processes engaged in the on-line control of behavior access to a synthetic world-space as their informational base. The difficulties encountered in the case of the well developed brains of cephalopods only multiply on posing the question of the final lower limits to which consciousness might be traced in the animal kingdom. Here unavoidable criterial issues regarding the extent of centralization and integration of sensory, motivational and other factors needed to qualify for possession of a ‘‘reality space’’ mechanism arise to confound judgement. It was noted earlier that in principle the complexity of the contents of consciousness have no bearing on the issue of whether a state of consciousness as such is present or not. For a conscious state to be present it suffices that one find oneself in the presence of any object whatsoever, however vaguely defined (Merker, 1997). That is, a bipartite ‘‘reality space’’ scheme omitting an object-like representation of the body from the reality arena of consciousness is in principle conceivable. The exact minimal limits of neural mechanisms needed to sustain such a bipartite representation is at this point an open question, as is the question of whether such a minimal arrangement would ever evolve in nature without including a representation of a spatialized body representation. According to the present proposal the selection pressure that promoted a ‘‘reality space’’ mechanism is after all the need to guide a body in space efficiently and without encumbrance from sensory preliminaries and motor sequels. From this the inclusion of a body representation in the reality space follows naturally. This may, however, be an unnecessarily ‘‘vertebratocentric’’ perspective. The extent of spatialization of the body representation in a ‘‘reality space’’ scheme is presumably related to the extent to which central decision processes control different parts of the body separately and selectively with respect to the surroundings. Adopt for a moment the perspective of a hover-fly. During flight its entire body moves essentially as a rigid unit (Collett & Land, 1975). It might therefore in principle be represented as a single spatial vector for control purposes. This might allow the body representation to be collapsed into the decision functions themselves, leaving a disembodied motivated agent facing a visual world stabilized by means of compensatory signals drawn from motor commands of flight control or other sources. If so, the result would be a bipartite ‘‘reality space’’ mechanism. This too might conceivably qualify as consciousness, if one insists on a minimum criterion involving a decision-making node equipped with an object-realm (however vaguely defined), and can specify the conditions of integration between these two that would place the decision node ‘‘in the presence of’’ an object. For now, suffice it to have posed the question in this extreme form.

7. Conclusion At the end of this path of successive simplification we return once more to the earthworm with which we started, by suggesting that the ultimate evolutionary anlage of the ‘‘reality space’’ scheme of consciousness is the first central representation of the kind of mechanism that allows the earthworm to discount cutaneous afference produced by self-motion as a stimulus for defensive withdrawal. To do so, such a representation must in one way or another represent a distinction

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between self and something else within one representational space, short of which it cannot embody even a minimal criterial definition of consciousness. Further than so it is not possible to reduce the issue without losing consciousness altogether. It is time to remind ourselves of the selection pressure which here has been proposed as the fundamental reason giving rise to the issue as well as reality of consciousness in the first place. That ultimate cause was the utility, for central decision and control purposes, of disentangling target-related guidance of behavior from movementproduced contamination of sensory information as well as from the complexities of muscular control. Given the potential gains achievable by doing so, consciousness has evolved as a solution to the neural logistics problems of mobile animals with centralized brains faced with managing the informational requirements of sophisticated orientation to their surroundings. For now, a better understanding of the neural architecture of the reality space embodying that solution would seem to be a more pressing question than an exact determination of the lowest level at which something qualifying as such a space might be detected in phylogeny. 8. Note added in proof Evidence for a direct collicular role in target selection—a crucial aspect of core control system function as conceived here—has accumulated since this paper was submitted (see R. M. McPeek & E. L. Keller (2004). Deficits in saccade target selection after inactivation of the superior colliculus. Nature Neuroscience, 7, 757-763 and R. J. Krauzlis, D. Liston & C. D. Carello (2004). Target selection and the superior colliculus: goals, choices and hypotheses. Vision Research, 44, 1445–1451 and references therein). The presence of a common intermediate system for target acquisition organized in Cartesian coordinates in the midbrain tegmentum (T. Masimo (1992). Brainstem control of orienting movements: Intrinsic coordinate systems and underlying circuitry. Brain, Behavior and Evolution, 40, 98–111) also bears on the present proposal, as does the presence of cortex-like gamma band oscillations in the superior colliculus (Brecht M, Goebel R, Singer W, Engel AK (2001). Synchronization of visual responses in the superior colliculus of awake cats. Neuroreport, 12, 43–47).

Acknowledgments I am indebted to the late Eugene Sachs for the basics of the perspective on consciousness elaborated in the present paper, and for the ‘‘respiratory control’’ example more specifically. I am also indebted to Guy Madison for numerous perceptive comments which have helped me improve the exposition. Part of my work on this manuscript was supported by a grant from the Bank of Sweden Tercentenary Foundation. References Allport, D. A. (1987). Selection for action: Some behavioral and neurophysiological considerations of attention and action. In H. Heuer & A. F. Sanders (Eds.), Perspectives on perception and action (pp. 395–419). Hillsdale, NJ: Erlbaum.

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