Thurston C. Lacalli's research while affiliated with University of Victoria and other places

The relationship between consciousness and individual agency is examined from a bottom-up evolutionary perspective, an approach somewhat different from other ways of dealing with the issue, but one relevant to the question of animal consciousness. Two ways are identified that would decouple the two, allowing consciousness of a limited kind to exist without agency: (1) reflex pathways that incorporate conscious sensations as an intrinsic component (InCs), and (2) reflexes that are consciously conditioned and dependent on synaptic plasticity but not memory (CCRs). Whether InCs and CCRs exist as more than hypothetical constructs is not clear, and InCs are in any case limited to theories where consciousness depends directly on EM field-based effects. Consciousness with agency, as we experience it, then belongs in a third category that allows for deliberate choice of alternative actions (DCs), where the key difference between this and CCR-level pathways is that DCs require access to explicit memory systems whereas CCRs do not. CCRs are nevertheless useful from a heuristic standpoint as a conceptual model for how conscious inputs could act to refine routine behaviors while allowing evolution to optimize phenomenal experience (i.e., qualia) in the absence of individual agency, a somewhat counterintuitive result. However, so long as CCRs are not a required precondition for the evolution of memory-dependent DC-level processes, the later could have evolved first. If so, the adaptive benefit of consciousness when it first evolved may be linked as much to the role it plays in encoding memories as to any other function. The possibility that CCRs are more than a theoretical construct, and have played a role in the evolution of consciousness, argues against theories of consciousness focussed exclusively on higher-order functions as the appropriate way to deal with consciousness as it first evolved, as it develops in the early postnatal period of life, or with the conscious experiences of animals other than ourselves. An evolutionary perspective also resolves the problem of free will, that it is best treated as a property of a species rather than the individuals belonging to that species whereas, in contrast, agency is an attribute of individuals.

The Middle Cambrian fossil Pikaia has a regular series of vertical bands that, assuming chordate affinities, can be interpreted as septa positioned between serial myotomes. Whether Pikaia has a notochord and nerve cord is less certain, as the dorsal organ, which has no obvious counterpart in living chordates, is the only clearly defined axial structure extending the length of the body. Without a notochord to serve as a reference point, the location of the nerve cord is then conjectural, which begs the question of how a dorsal neural center devoted to somite innervation would first have arisen from a more diffuse ancestral plexus of intraepithelial nerves. This question is examined using hemichordates as a reference point, first for the information they provide on the organization of the ancestral deuterostome nervous system, and second, extending the analysis of E. E. Ruppert, to explain why neural infoldings like the enteropneust collar cord would first have evolved. Both implicate the medial surface of the anterior-most part of the metacoel as the likely site for the evolution of the first somites. The analysis highlights the importance of the somatobranchial condition in chordates, meaning the linkage between the anterior trunk, hox1 expression, and the beginning of the gill series and somites. This feature is arguably a valid criterion by which to assess extinct taxa from the Cambrian that resemble chordates (e.g., vetulicolians and yunnanozoans), but may be unrelated to them. In a more speculative vein, the nature of the dorsal organ is discussed, including the possibility that it is an expanded neural tube combining neural and support functions in one structure.

Few of the many theories devised to account for consciousness are explicit about the role they ascribe to evolution, and a significant fraction, by their silence on the subject, treat evolutionary processes as being, in effect, irrelevant. This is a problem for biological realists trying to assess the applicability of competing theories of consciousness to taxa other than our own, and across evolutionary time. Here, as an aid to investigating such questions, a consciousness “machine” is employed as conceptual device for thinking about the different ways ontology and evolution contribute to the emergence of a consciousness composed of distinguishable contents. A key issue is the nature of the evolutionary innovations required for any kind of consciousness to exist, specifically whether this is due to the underappreciated properties of electromagnetic (EM) field effects, as in neurophysical theories, or, for theories where there is no such requirement, including computational and some higher-order theories (here, as a class, algorithmic theories), neural connectivity and the pattern of information flow that connectivity encodes are considered a sufficient explanation for consciousness. In addition, for consciousness to evolve in a non-random way, there must be a link between emerging consciousness and behavior. For the neurophysical case, an EM field-based scenario shows that distinct contents can be produced in the absence of an ability to consciously control action, i.e., without agency. This begs the question of how agency is acquired, which from this analysis would appear to be less of an evolutionary question than a developmental one. Recasting the problem in developmental terms highlights the importance of real-time feedback mechanisms for transferring agency from evolution to the individual, the implication being, for a significant subset of theories, that agency requires a learning process repeated once in each generation. For that subset of theories the question of how an evolved consciousness can exist will then have two components, of accounting for conscious experience as a phenomenon on the one hand, and agency on the other. This reduces one large problem to two, simplifying the task of investigation and providing what may prove an easier route toward their solution.

This paper elaborates on a proposal for mapping a configuration space for selector circuits (SCs), defined as the subset of neural correlates of consciousness (NCCs) responsible for evoking particular qualia, to its experiential counterpart, experience-space (E-space), as part of an investigation into the nature of conscious experience as it first emerged in evolution. The dimensionality of E-space, meaning the degrees of freedom required to specify the properties of related sets of qualia, is at least two, but the utility of E-space as a hypothetical construct is much enhanced by assuming it is a large dimensional space, with at least several times as many dimensions as there are categories of qualia to occupy them. Phenomenal consciousness can then be represented as having originated as one or more multidimensional ur-experiences that combined multiple forms of experience together. Taking this as a starting point, questions concerning evolutionary sequence can be addressed, including how the quale best suited to a given sensory modality would have been extracted by evolution from a larger set of possibilities, a process referred to here as dimensional sorting, and how phenomenal consciousness would have been experienced in its earliest manifestations. There is a further question as to whether the E-space formulation is meaningful in analytical terms or simply a descriptive device in graphical form, but in either case it provides a more systematic way of thinking about early stages in the evolution of consciousness than relying on narrative and conjecture alone.

This is a brief account of Turing’s ideas on biological pattern and the events that led to their wider acceptance by biologists as a valid way to investigate developmental pattern, and of the value of theory more generally in biology. Periodic patterns have played a key role in this process, especially 2D arrays of oriented stripes, which proved a disappointment in theoretical terms in the case of Drosophila segmentation, but a boost to theory as applied to skin patterns in fish and model chemical reactions. The concept of “order from fluctuations” is a key component of Turing’s theory, wherein pattern arises by selective amplification of spatial components concealed in the random disorder of molecular and/or cellular processes. For biological examples, a crucial point from an analytical standpoint is knowing the nature of the fluctuations, where the amplifier resides, and the timescale over which selective amplification occurs. The answer clarifies the difference between “inelegant” examples such as Drosophila segmentation, which is perhaps better understood as a programmatic assembly process, and “elegant” ones expressible in equations like Turing’s: that the fluctuations and selection process occur predominantly in evolutionary time for the former, but in real time for the latter, and likewise for error suppression, which for Drosophila is historical, in being lodged firmly in past evolutionary events. The prospects for a further extension of Turing’s ideas to the complexities of brain development and consciousness is discussed, where a case can be made that it could well be in neuroscience that his ideas find their most important application.

The similarities between amphioxus and vertebrate brains, in their regional subdivision, cell types and circuitry, make the former a useful benchmark for understanding the evolutionary innovations that shaped the latter. Locomotory control systems were already well developed in basal chordates, with the ventral neuropile of the dien-mesencephalon serving to set levels of activity and initiate locomotory actions. A chief deficit in amphioxus is the absence of complex vertebrate-type sense organs. Hence, much of vertebrate story is one of progressive improvement both to these and to sensory experience more broadly. This has two aspects: (i) anatomical and neurocircuitry innovations in the organs of special sense and the brain centres that process and store their output, and (ii) the emergence of primary consciousness, i.e. sentience. With respect to the latter, a bottom up, evolutionary perspective has a different focus from a top down human-centric one. At issue: the obstacles to the emergence of sentience in the first instance, the sequence of addition of new contents to evolving consciousness, and the homology relationship between them. A further question, and a subject for future investigation, is how subjective experience is optimized for each sensory modality. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Conscious experience can be treated as a complex unified whole, but to do so is problematic from an evolutionary perspective if, like other products of evolution, consciousness had simple beginnings, and achieved complexity only secondarily over an extended period of time as new categories of subjective experience were added and refined. The premise here is twofold, first that these simple beginnings can be investigated regardless of whether the ultimate source of subjective experience is known or understood, and second, that of the contents known to us, the most accessible for investigation will be those that are, or appear, most fundamental, in the sense that they resist further deconstruction or analysis. This would include qualia as they are usually defined, but excludes more complex experiences (here, formats) that are structured, or depend on algorithmic processes and/or memory. Vision and language for example, would by this definition be formats. More formally, qualia, but not formats, can be represented as points, lines, or curves on a topological experience space, and as domains in a configuration space representing a subset of neural correlates of consciousness, the selector circuits (SCs), responsible for ensuring that a particular experience is evoked rather than some other. It is a matter of conjecture how points in SC-space map to experience space, but both will exhibit divergence, insuring that a minimal distance separates points in experience space representing different qualia and the SCs that evoke them. An analysis of how SCs evolve over time is used to highlight the importance of understanding patterns of descent among putative qualia, i.e., their homology across species, and whether this implies descent from an ancestral experience, or ur-quale, that combines modes of experience that later came to be experienced separately. The analysis also provides insight into the function of consciousness as viewed from an evolutionary perspective, defined here in terms of the access it allows to regions of SC-space that would otherwise be unavailable to real brains, to produce consciously controlled behaviors that could otherwise not occur.

Heterochrony has played a key role in the evolution of invertebrate larval types, producing “head larvae” in diverse taxa, where anterior structures are accelerated and specialized at the expense of more caudal ones. For chordates, judging from amphioxus, the pattern has been more one of repeated acceleration of adult features so that they function earlier in development, thus converting the ancestral larva, whether it was a head larva or not, into something progressively more chordate-like. Recent molecular data on gene expression patterns in the anterior nerve cord of amphioxus point to a similar process being involved in the origin of the telencephalon. As vertebrates evolved, a combination of acceleration and increasing egg size appears here to have allowed the development of a structure that would originally have emerged only gradually in the post-embryonic phase of the life history to be compressed into embryogenesis. The question then is what, in functional terms, makes the telencephalon so important to the survival of post-embryonic ancestral vertebrates that this was adaptively advantageous. A better understanding of the function this brain region performs in amphioxus may help provide the answer.

Amphioxus has astroglia‐ and radial glia‐like cells. Neurons and glia arise from different precursor populations. Multipotent radial glia‐like progenitors were likely present in the last common ancestor of deuterostomes. Neurons and glia arise from different precursor populations. Multipotent radial glia‐like progenitors were likely present in the last common ancestor of deuterostomes. Glial cells play important roles in the development and homeostasis of metazoan nervous systems. However, while their involvement in the development and function in the central nervous system (CNS) of vertebrates is increasingly well understood, much less is known about invertebrate glia and the evolutionary history of glial cells more generally. An investigation into amphioxus glia is therefore timely, as this organism is the best living proxy for the last common ancestor of all chordates, and hence provides a window into the role of glial cell development and function at the transition of invertebrates and vertebrates. We report here our findings on amphioxus glia as characterized by molecular probes correlated with anatomical data at the transmission electron microscopy (TEM) level. The results show that amphioxus glial lineages express genes typical of vertebrate astroglia and radial glia, and that they segregate early in development, forming what appears to be a spatially separate cell proliferation zone positioned laterally, between the dorsal and ventral zones of neural cell proliferation. Our study provides strong evidence for the presence of vertebrate‐type glial cells in amphioxus, while highlighting the role played by segregated progenitor cell pools in CNS development. There are implications also for our understanding of glial cells in a broader evolutionary context, and insights into patterns of precursor cell deployment in the chordate nerve cord.