The evolutionary and genetic origins of consciousness in the Cambrian Period over 500 million years ago

Abstract

Vertebrates evolved in the Cambrian Period before 520 million years ago, but we do not know when or how consciousness arose in the history of the vertebrate brain. Here we propose multiple levels of isomorphic or somatotopic neural representations as an objective marker for sensory consciousness. All extant vertebrates have these, so we deduce that consciousness extends back to the group's origin. The first conscious sense may have been vision. Then vision, coupled with additional sensory systems derived from ectodermal placodes and neural crest, transformed primitive reflexive systems into image forming brains that map and perceive the external world and the body's interior. We posit that the minimum requirement for sensory consciousness and qualia is a brain including a forebrain (but not necessarily a developed cerebral cortex/pallium), midbrain, and hindbrain. This brain must also have (1) hierarchical systems of intercommunicating, isomorphically organized, processing nuclei that extensively integrate the different senses into representations that emerge in upper levels of the neural hierarchy; and (2) a widespread reticular formation that integrates the sensory inputs and contributes to attention, awareness, and neural synchronization. We propose a two-step evolutionary history, in which the optic tectum was the original center of multi-sensory conscious perception (as in fish and amphibians: step 1), followed by a gradual shift of this center to the dorsal pallium or its cerebral cortex (in mammals, reptiles, birds: step 2). We address objections to the hypothesis and call for more studies of fish and amphibians. In our view, the lamprey has all the neural requisites and is likely the simplest extant vertebrate with sensory consciousness and qualia. Genes that pattern the proposed elements of consciousness (isomorphism, neural crest, placodes) have been identified in all vertebrates. Thus, consciousness is in the genes, some of which are already known.

Full text

HYPOTHESIS AND THEORY ARTICLE
published: 04 October 2013
doi: 10.3389/fpsyg.2013.00667
The evolutionary and genetic origins of consciousness in
the Cambrian Period over 500 million years ago
Todd E. Feinberg
1
*
and Jon Mallatt
2
1
Neurology and Psychiatry, Albert Einstein College of Medicine and Beth Israel Medical Center, New York, NY, USA
2
School of Biological Sciences, Washington State University, Pullman, WA, USA
Edited by:
Anil K. Seth, University of Sussex,
UK
Reviewed by:
Anil K. Seth, University of Sussex,
UK
David B. Edelman, Bennington
College, USA
Bernard J. Baars, The
Neurosciences Institute, USA
*Correspondence:
Todd E. Feinberg, Yarmon
Neurobehavior and Alzheimer’s
Disease Center, Beth Israel Medical
Center, First Avenue at 16th Street,
New York, NY 10003, USA
e-mail: tfeinber@chpnet.org
Vertebrates evolved in the Cambrian Period before 520 million years ago, but we do not
know when or how consciousness arose in the history of the vertebrate brain. Here
we propose multiple levels of isomorphic or somatotopic neural representations as an
objective marker for sensory consciousness. All extant vertebrates have these, so we
deduce that consciousness extends back to the group’s origin. The first conscious sense
may have been vision. Then vision, coupled with additional sensory systems derived
from ectodermal placodes and neural crest, transformed primitive reflexive systems into
image forming brains that map and perceive the external world and the body’s interior.
We posit that the minimum requirement for sensory consciousness and qualia is a brain
including a forebrain (but not necessarily a developed cerebral cortex/pallium), midbrain,
and hindbrain. This brain must also have (1) hierarchical systems of intercommunicating,
isomorphically organized, processing nuclei that extensively integrate the different senses
into representations that emerge in upper levels of the neural hierarchy; and (2) a
widespread reticular formation that integrates the sensory inputs and contributes to
attention, awareness, and neural synchronization. We propose a two-step evolutionary
history, in which the optic tectum was the original center of multi-sensory conscious
perception (as in fish and amphibians: step 1), followed by a gradual shift of this center
to the dorsal pallium or its cerebral cortex (in mammals, reptiles, birds: step 2). We
address objections to the hypothesis and call for more studies of fish and amphibians.
In our view, the lamprey has all the neural requisites and is likely the simplest extant
vertebrate with sensory consciousness and qualia. Genes that pattern the proposed
elements of consciousness (isomorphism, neural crest, placodes) have been identified
in all vertebrates. Thus, consciousness is in the genes, some of which are already known.
Keywords: isomorphic/somatotopic neural representations, sensory images, qualia, neural crest and placodes,
lamprey, genes of consciousness, optic tectum and consciousness, thalamocortical complex
INTRODUCTION
But no matter how the form may vary, the fact that an organism
has conscious experience at all means, basically, that there is some-
thing it is like to be that organism. ...fundamentally an organism
has conscious mental states if and only if there is something that
it is like to be that organism - something it is like for the organ-
ism. We may call this the subjec tive character of experience (Nagel,
1974, p. 436).
Although there are many aspects to the nature of consciousness,
this paper focuses on the neurological basis and evolutionary
origins of sensory consciousness. Sensory consciousness is akin
to concepts such as phenomenal consciousness (Revonsuo, 2006,
2010; Boly and Seth, 2012), primary consciousness (Edelman,
1989), subjectivity (Nagel, 1989; Searle, 1992, 1997; Tye, 2000;
Metzinger, 2003; Velmans, 2009; Feinberg, 2012), or the experi-
ence of qualia (Churchland and Churchland, 1981; Jackson, 1982;
Levine, 1983; Dennett, 1988, 1991; Flanagan, 1992; Kirk, 1994;
Chalmers, 1995, 1996, 2010; McGinn, 1999; Metzinger, 2003).
Other studies explore the evolutionary origin of consciousness
in memory and learning, for goal-directed actions and behav-
iors, or in arousal and emotions (Ginsburg and Jablonka, 2010,
2011; Mashour and Alkire, 2013), but again, our focus will be on
sensory experience.
This is because the subjective nature of qualia is so impor-
tant. Chalmers sees it as the central issue of the problem of
consciousness:
If any problem qualifies as the problem of consciousness, it is this
one. In this central sense of “consciousness”, an organism is con-
scious if there is something it is like to be that organism, and a
mental state is conscious if there is something it is like to be in that
state. Sometimes terms such as “phenomenal consciousness” and
“qualia” are also used here, but I find it more natur al to speak of
“conscious experience” or simply “experience” (Chalmers, 1995,
p. 201).
The current inabilit y to understand such experiences is called
the explanatory gap (see Block, 2009), and Crick and Koch agree
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
that the puzzle of sensory subjectivity must be solved for progress
to be made:
The most difficult aspect of consciousness is the so-called ‘hard
problem’ of qualia,—the redness of red, the painfulness of pain,
and so on. No one has produced any plausible explanation as to
how the experience of the redness of red could arise from the
actions of the brain (Crick and Koch, 2003, p. 119).
Here we take on this fundamental problem from the non-
traditional perspective of evolutionary, developmental, and
genetic neurobiology.
Revonsuo’s definition of phenomenal consciousness expands
the description of the subjective, phenomenal, and sensory
aspects of consciousness:
Phenomenal consciousness is the current presence of subjective
experiences, or the having of subjective experiences. An organism
possesses phenomenal consciousness if there is any type of sub-
jective experience currently present for it. The mere occurrence
or presence of any experience is the necessary and minimally suf-
ficient condition for phenomenal consciousness. For any entity
to possess primary phenomenal consciousness only requires that
there are at least some patterns – any patterns at all – of subjective
experience present-for-it. It is purely about the having of any sorts
of patterns of subjective experience, whether simple or complex,
faint or vivid, meaningful or meaningless, fleeting or lingering
(Revonsuo, 2006, p. 37).
In this paper, when we refer to “sensory consciousness” we
are referring to these unique, phenomenal, subjective features
of consciousness (Feinberg, 2009, 2011, 2012). But if we are
to deepen our understanding of the evolutionary origins and
neurobiological basis of sensory consciousness, we must first
face the difficult task of tr anslating descriptions of neurologi-
cal structure and function into concepts that describe subjective
experience.
What organisms are likely to possess phenomenal conscious-
ness or subjective states of awareness? Clearly, whether one deems
an animal “conscious” depends upon what criteria are employed
(Cartmill, 2000; Griffin, 2000; Butler et al., 2005; Edelman et al.,
2005; Seth et al., 2005; Edelman and Seth, 2009). The question of
consciousness has been studied in intellectually advanced, large-
brained animals such as non-human primates, birds, octopuses,
and squids (e.g., Pennisi, 1999; Butler et al., 2005; Edelman et al.,
2005; Seth et al., 2005; Butler, 2008a; Mather, 2008; Edelman
and Seth, 2009), but we wish to explicate the simplest neural
architecture most relevant to human consciousness and there-
fore will focus on the earliest appearance of sensory consciousness
in vertebrate-craniate evolution (Northcutt, 1996a,b; Hodos and
Butler, 1997; Nieuwenhuys and Nicholson, 1998; Butler, 2000;
Holland and Holland, 2001; Butler and Hodos, 2005; Lacalli,
2008a,b; Fritzsch and Glover, 2009; Glover and Fritzsch, 2009;
Kaas, 2009). Because usage of the names “vertebrate” vs. “cra-
niate” is confused and in flux (Kardong, 2012), we will keep
things simple by using both names synonymously to designate
the group of animals with a vertebral column and skull. These are
the fish, amphibians, reptiles, birds, and mammals of common
parlance.
While no single concept or approach to sensory consciousness
can subsume all others, we take as a starting point the ques-
tion of how an essentially neurological concept—the concept of
“somatotopic,” “topographic,” and “isomorphic” sensory maps or
representations—can be translated into simple ideas or terms that
have a clear meaning from the standpoint of subjective awareness,
without getting too deeply ent renched in the many complex and
thorny philosophical issues that this approach might entail.
“Isomorphic map” (Hodos and Butler, 1997)isageneralterm
for neural representations that are organized spatially accord-
ing to different points in the sensory field or in the outside
world being sensed (retinotopic, somatotopic, nociceptive, or
cochleotopic and thereby tonotopic) as well as the non-spatially
organized, chemotopically mapped representations (olfactory
and gustatory) (Barlow, 1981, 1986; Northcutt and Kaas, 1995;
Kaas, 1997; Leon and Johnson, 2003; Shepherd, 2007; Thivierge
and Marcus, 2007; Gottfried, 2010). It is generally held that
isomorphic maps are essential to sensory functioning in ver-
tebrates: These maps persist through a hierarchy of successive
and interconnected processing stations, with the topographical
organization becoming progressively more complex in the higher
stations in the brain (Kaas, 1997). Here we propose that certain
sorts of complex, integrated isomorphic representations are asso-
ciated with conscious scenes, and the purpose of this paper is to
explore the implications of this assumption across a larger range
of vertebrate animals, and in considerably more biological detail,
than has been done previously.
Although the isomorphic map is a fundamental and shared
trait, the different sensory systems have some special features
and variations in their maps. For example, while the somato-
topic maps for “touch” roughly preserve the spatial relationship
between their respective receptor surfaces and their central neural
representations, some of these maps, such as in the somatosen-
sor y homunculus within SI of the postcentral gyrus of the mam-
malian cerebral cortex, are in reality splits or gross distortions
of the body surface, reflecting additional features such as the
greater density of peripheral innervation in some body regions
(Kaas, 1997; Merker, 2007). Another map, in the vestibular cor-
tex and involved with the sense of equilibrium, is both genuinely
somatotopic (Grusser et al., 1990; Lopez and Blanke, 2011)and
“directionally isomorphic,” consciously sensing movements of the
bodythrough3Dspace(Chen et al., 2010). The chemotopic maps
of olfactory and gustatory functioning are spatial at only some
levels of their sensory pathways and not spatially organized at
other levels (Sewards and Sewards, 2001; Rawson and Yee, 2006;
Hara, 2007; Sosulski et al., 2011; Jacobs, 2012), so it is best to refer
to these maps as isomorphic alone, still representing a hierarchi-
cal neural mapping for the construction of a sensory image (i.e.,
of different odorants or tastants).
We propose that, when considered from the point of view of
the conscious human or non-human animal, the high-order iso-
morphic neural-representations are experienced as sensory mental
images. We use the term “sensory mental image” to describe
those aspects of phenomenal consciousness that are the direct and
immediate result of the brain’s processing of sensor y information,
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
much the same way as Gerald Edelman defines primary con-
sciousness as “the state of being mentally aware of things in the
world—of having mental images in the present” (Edelman, 1992).
Other studies have also suggested that isomorphic maps are crit-
ical to the creation of sensory consciousness (Edelman, 1989;
Damasio, 1999; Feinberg, 2009, 2011, 2012). Note that this use of
the term “mental image” is not the same as “mental imagery” that
results from mental imagining in the absence of an immediate
stimulus. By our reasoning, an organism with a nervous system
that tr anslates its sensory arrays into mental images through cen-
tral processing (see Table 1) possesses at least a minimal form of
sensory, phenomenal, or primary consciousness. Note from the
table that conscious images would only emerge with contribu-
tions from the third- and higher orders in mammals (cerebral
cortex), and the second order in fishes and amphibians (optic
tectum).
In this paper, we deduce that consciousness evolved in the
earliest vertebrates in the Cambrian, the oldest geologic period
with abundant fossil evidence for complex animals (Erwin and
Valentine, 2013). A few other authors have also proposed that
changes at this time were associated with the origin of con-
sciousness. Hameroff (1998) suggested that consciousness first
evolved in the Cambrian in simple worms, urchins, or even in
one-celled organisms (suctorians), due to quantum effects at the
level of microtubules in their cells. Ginsburg and Jablonka (2010,
2011) argued for an even earlier origin of consciousness than we
do, in the pre-Cambrian, Ediacaran Period with the very first
appearance of worm-like bilaterian animals; and that this con-
sciousness coincided with the evolution of associative learning
and memory. With reference to Hameroff (1998) and Ginsburg
and Jablonka (2010, 2011), we will argue that simple bilaterians
or one-celled creatures are not conscious because consciousness
requires a more-complex nervous system. Additionally, with ref-
erence to Ginsburg and Jablonka we argue that learning and
memory are well documented in simple animals like worms and
Aplysia (snail-like sea slug: Hawkins et al., 2006; Kandel, 2009),
Table 1 | A simplified summary of some of the major sensory receptors and isomorphic pathways leading to sensory mental images.
Isomorphic templates
Sensory domain, receptor
type
First order multipolar Second order Third order* isomorphism,
image type
Vision, photoreceptors: rods
and cones
Retina = retinal ganglion
cells
Thalamus = lateral geniculate,
optic tectum*
Primary visual cortex (V1),
retinotopic,
visual images
Somesthetic senses,
mechanoreceptors
Dorsal column nuclei
(trunk), sensory
trigeminal nerve nuclei
(face)
Thalamus = VPL and VPM,
tectum*
Primary somatosensory cortex (SI),
somatotopic,
somatosensory images
Pain, nociceptors Dorsal horn lamina I
(trunk), sensory
trigeminal nuclei (face)
Thalamus = VPL/VPM, VMpo,
tectum*
SI and insula-anterior cingulate,
somatotopic-homeostatic,
pain images
Olfaction,
chemoreceptors:
olfactory sensory neurons
Olfactory bulb =
glomeruli: mitral cells
Olfactory cortex Orbitofrontal cortex,
chemotopic,
olfactory images.
Hippocampus and dentate gyrus,
olfactory images
Gustation, chemoreceptors:
taste cells
Gustatory nucleus Thalamus = VPMpc, tectum* Anterior insula/frontal operculum,
chemotopic,
taste images
Audition, mechanoreceptors:
inner hair cells
Cochlear nuclei Thalamus = medial geniculate,
inferior colliculus, tectum
*
Primary auditory, c ortex, tonotopic,
auditory images
Equilibrium,
mechanoreceptors: hair cells
Vestibular nuclei Thalamus = multiple thalamic
nuclei, tectum
*
Primary vestibular cortex
(parieto-insular vestibular cortex:
PIVC),
images of body position and motion
*
Here the third-order telencephalic areas are listed for mammals, but higher levels also exist: Heteromodal association cortices (also designated as high-order
association cortex, polymodal cortex, multimodal cortex, polysensory areas, and supramodal cortex) serve as fourth-order integration zones, and inthehumanbrain
they include the posterior and anterior parietal cortex, lateral temporal cortex, prefrontal cortex, and portions of the parahippocampal gyrus (Mesulam, 2000). In
birds, the third and fourth orders also are in the pallium (Butler et al., 2005, 2011). In fish and amphibians, by contrast, the optic tectum is where the isomorphic
visual, somatosensory, auditory, vestibular and nociceptive templates and images are best documented, as are the multimodal images (Echteler, 1985; McHaffie
et al., 1989; Stein and Meredith, 1993; Merker, 2005, 2007; Dicke and Roth, 2009; Wullimann and Vernier, 2009a).
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
yet according to our hypothesis the y are not conscious. In fact,
even computers have memory and can be programmed to learn
without consciousness.
We avoid the intricacies of cognition- and quantum-based
approaches to consciousness by focusing on sensory experience,
which seems to be a more solvable problem in terms of current
neurobiological knowledge. In fact, our tactic of analyzing the
basis and origins of isomorphic sensory images has the unique
advantage of triangulating between the neurobiological domain
(of somatotopy, isomorphism, neurohierarchical pathways), neu-
ropsychological domain (of sensory images) and neurophilo-
sophical domain (of subjective experience and the hard problem)
and thus could serve as a versatile analytic tool with wide applica-
tion to these various approaches. Using multi-level, isomorphic
sensor y representations as an objective “marker” for the pres-
ence of sensory consciousness, we will consider: How and when
did isomorphic sensory images evolve? And what are the simplest
extant vertebrates that have them? Finally, we will consider the
implications of this analysis for a neuroscience and a genetics of
consciousness.
THE BIRTH OF BRAINS
Members of the phylum Chordata, including humans, are char-
acterized by the presence at some point in their life cycle of a
notochord (an elongated cellular chord that provides structural
support for the animal’s body) and a dorsal nerve cord. The chor-
dates consist of three subphyla: Vertebrata, Cephalochordata, and
Urochordata or tunicates (Figure 1)(Kardong, 2012). The verte-
brates include the jawless hagfish and lampreys (cyclostomes), as
well as the jawed vertebrates (gnathostomes). The gnathostomes
FIGURE 1 | Tree and timeline of the evolution of vertebrates. Note the
subgroups of the chordates. The vertebrate/craniate lineage evolved during
the Cambrian Period approximately 560–520 million years ago (blue bar on
the timeline). The two basic subdivisions of vertebrates are the jawless
cyclostomes, namely hagfish and lamprey, and the jawed gnathostomes, to
which we humans belong. The lamprey is thought to retain more features
of the ancestral first vertebrate than do hagfish or gnathostomes.
consist of the jawed fish (cartilaginous and bony fish), amphib-
ians, reptiles, birds, and mammals. The reptiles, birds, and mam-
mals comprise the amniotes, so all the other vertebrates are called
anamniotes (fish and amphibians). The first amniotes appeared
in the Late Paleozoic Era about 350–330 mya, and fossils reveal
they were extremely reptile-like, even lizard-like in appearance.
Later, about 315 mya, the amniotes split into two lines: the synap-
sids (mammal-like reptiles and later, their mammal descendants);
and the sauropsids, which include the living reptiles and the birds
(“feathered dinosaurs”) (Kemp, 1982; Benton and Donoghue,
2007; Organ et al., 2007). Actually, the position of turtles among
reptiles is uncertain because some evidence places turtles in
sauropsids and other evidence indicates they arose before the
sauropsid/synapsid split (Mallatt and Winchell, 2007).
Turning to the non-vertebrate chordates, which are informally
called protochordates, the tunicate urochordates (also known as
sea squirts) have a free-sw imming larval phase during which they
possess the chordate-defining notochord and nerve cord, and a
bag-like adult form that is sessile (non-mobile) and anchored
in one place on the ocean bottom (Burighel and Cloney, 1997).
The cephalochordates ( lancelets or amphioxus) are 4–6 cm long
fish-shaped animals in which both the larvae and adults swim
well and whose notochord and nerve cord persist their entire
lives (Ruppert, 1997; Nieuwenhuys and Nicholson, 1998; Allman,
1999; Butler, 2000; Butler and Hodos, 2005; Fritzsch and Glover,
2009; Glover and Fritzsch, 2009; Kardong, 2012). The adults live
burrowed in ocean sediment.
Molecular and neuroanatomical studies indicate that
amphioxus has brain structures (Figure 2A) that are homologous
to the diencephalic forebrain and the hindbrain of vertebrates,
and perhaps also a small midbrain (Lacalli, 1996a,b, 2004, 2005,
2008a,b, 2010; Butler, 2000; Holland and Chen, 2001; Wicht and
Lacalli, 2005). For instance, in larval amphioxus the cerebral
vesicle located at the rostral end of the neuraxis contains several
structures that Lacalli has identified as homologues of dien-
cephalic structures of most craniates, and an unpaired frontal eye
in the midline that is the homologue of vertebrates’ paired eyes
(also see Vopalensky et al., 2012).
Studies suggest that cephalochordates conserve a wider array
of primitive chordate characteristics than do tunicates and there-
fore that amphioxus is the best available model for the proximate
ancestor of the vertebrates (Holland and Chen, 2001; Mallatt,
2009; Mallatt and Holland, 2013). In addition, Putnam et al.
(2008) support the view that amphioxus reveals the critical fea-
tures of the genome of the last common ancestor of all chordates
and that a pre-Cambrian cephalochordate-like ancestor gave rise
tomoderncephalochordatesaswellastourochordatesand
vertebrates.
However, Glover and Fritzsch (2009) focusmoreonurochor-
dates. They note that the free-swimming larvae of most urochor-
dates have a simple central nervous system (Figure 2B) consisting
of a rostral ganglion with an ocellus (unpaired eye), a caudal gan-
glion, and a caudal nerve cord that are homologous to the craniate
diencephalon and eye, hindbrain, and spinal cord, respectively.
Although the urochordate brain has become specialized and even
reduced, Glover and Fritzsch (2009) say it evolved from a more
advanced ancestral brain because its bulged sub-parts are more
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
FIGURE 2 | Comparison of the brains of (A) larval amphioxus, (B) larval
tunicate Ciona intestinalis, and (C) the lamprey Lampetra fluviatilis.
In all three pictures, anterior is to the left. Based on Young (1962),
Nieuwenhuys (1972, 1977), Burighel and Cloney (1997), Nieuwenhuys and
Nicholson (1998), Fritzsch and Glover (2009),andGlover and Fritzsch (2009).
Only the lamprey has a well-delineated tripartite brain and the full suite of
neural-crest derivatives.
distinct than in the un-bulged, uniformly tube-shaped brain of
cephalochordates (compare Figures 2A,B). Further, while it was
long supposed that cephalochordates are the closest relatives (sis-
ter group) of the vertebrates, more recent molecular-phylogenetic
analyses suggest that urochordates instead are the sister group of
vertebrates and that the cephalochordates arose earlier (Bourlat
et al., 2006; Delsuc et al., 2006; Holland, 2007; Hall, 2008; Lacalli,
2008b; Lamb, 2011; Figure 1).
Protochordates lack some key vertebrate features. Their tiny
eyes do not form images (Lacalli, 2004; Lamb et al., 2007, 2008;
Lamb, 2011, 2013) and they lack a telencephalic forebrain; thus,
the camera eye and telencephalon seem to have been vertebrate
innovations (Holland and Chen, 2001; Fritzsch and Glover, 2009;
Figure 2C). For now, most experts stick with this straightfor-
ward interpretation of the facts (e.g., Lamb, 2013), even though
some new genetic and cellular evidence suggests the eyes of both
protochordate groups were secondarily simplified, implying the
first chordates had slightly more elaborate eyes (Lacalli, 2013;
Sestak et al., 2013). Another vertebrate feature is absent from
cephalochordates. Although somatosensory cells occur in small
clusters on their body surface (Lacalli, 2004), there are no dorsal
root ganglia anywhere along the neuraxis (Glover and Fritzsch,
2009). The evidence for an olfactory system is scanty in both
groups of protochordates (Lacalli, 2004; Graham and Shimeld,
2012).
In summary, the ancestral chordate nervous system probably
resembled that of modern cephalochordates and larval urochor-
dates and featured a primitive brain but lacked a telencephalon.
Its eye homologue sensed light but did not form an image. The
evolutionary elaboration of these features toward the vertebrate
state was the next critical stage in the origins of sensory images
and consciousness.
DATE OF ORIGIN OF CONSCIOUSNESS
When did this progression toward vertebrates and the hypothe-
sized dawn of vertebrate consciousness occur? The earliest con-
firmed vertebrate fossils date to 520 million years ago (mya), in
the early part of the Cambrian Period (which itself lasted from
about 541–488 mya) (Valentine, 2002; Shu et al., 2003; Erwin and
Valentine, 2013). Therefore, 520 mya is the most-recent possible
date. To deduce the older end of the interval, we note that the
first body fossils of any kind of Bilateria are 556 million years
old (Erwin and Valentine, 2013), Bilateria being the group of ani-
mals that includes the chordates and all the invertebrates except
sponges, jellyfish, and their relatives (see Figure 1). This makes
560 mya a reasonable estimate of the maximum age for the ver-
tebrate line, although “molecular clocks” that date the origins of
taxa by measuring rates of gene evolution place this earlier, at 605
mya (Erwin et al., 2011). The clock method, however, has been
challenged for producing unrealistically early t imes of origin for
animal phyla (Bromham, 2006), even with the refinements used
by Peterson et al. (2008), Erwin et al. (2011), and others. Thus,
we date the emergence of pre-vertebrates, vertebrates, and their
distinctive features to the interval of 560–520 mya (Figure 1).
KEY INNOVATIONS: NEURAL CREST, PLACODES, AND THE
ELABORATION OF SENSORY ORGANS
Perhaps the single most important innovation marking this tran-
sition to ver tebrates was the appearance of neural crest and
neural placodes (Gans and Northcutt, 1983; Northcutt, 1996a,b,
2005; Hall, 2008; Sauka-Speng ler and Bronner-Fraser, 2008). The
neural plate is a region of thickened ectoderm that forms longitu-
dinally on the dorsal surface of the developing vertebrate embryo
(Figure 3). Then, double-walled folds form at the anterior and
lateral regions of the neural plate, the inner walls of which give
rise to the neural crest cells while the lateral folds give rise to the
ectodermal or neurogenic placodes (Allman, 1999; Holland and
Chen, 2001; Holland and Holland, 2001; Baker, 2005; Schlosser,
2005, 2008; Donog hue et al., 2008; Hall, 2008, 2009; Graham and
Shimeld, 2012).
Neural crest cells mig rate into the head and trunk regions of
the body where they differentiate into v arious cell types includ-
ing some cranial sensor y neurons, all the sensory neurons in the
trunk, all ganglionic autonomic neurons, and all the pigment cells
called melanocytes. Placodes are thickened areas of epithelium
that differentiate into neural and non-neural structures. Cranial
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
FIGURE 3 | Development of the neural crest and placodes, near the
midline of the back. In vertebrates, double-walled folds form at the
anterior and lateral regions of the neural plate, the inner walls of which give
rise to the neural crest while the lateral folds give rise to the neurogenic
placodes.
neurogenic placodes give rise to paired peripheral organs of spe-
cial sense and contribute to the development of the olfactory
system (olfactory placodes that form the olfactory receptors), the
lens of the eye, the inner ear (otic placodes that form the hair-cell
receptors for hearing and equilibrium), the majority of cranial
sensory neurons, and the lateral line system of fish. The neu-
rons in the trigeminal ganglion (cranial nerve V) that transmit
sensations of touch, pain, and temperature from the face are of
combined neural crest and placodal origin, and the neurons of
the facial, glossopharyngeal, and vagus nerves that provide affer-
ent innervation for the taste buds are of placodal origin. Indeed,
the entire peripheral nervous system is derived from cells that
originate within the neural crest and cranial placodes (Holland
and Holland, 2001; Baker, 2005; Schlosser, 2005, 2008, 2010;
Donoghue et al., 2008; Hall, 2008, 2009; Graham and Shimeld,
2012). A minor exception is that all life stages of lampreys, and
the larvae of fish and amphibians, retain a few non-crest-derived
sensory neurons called Rohon-Beard cells. The cell bodies of these
exceptional neurons are not in the dorsal roots, but are inside
the spinal cord of the central nervous system, mirroring the con-
dition in amphioxus (Nieuwenhuys and Nicholson, 1998; Wicht
and Lacalli, 2005; Rossi et al., 2009).
Whether there are neural crest or placodal derivatives in non-
craniates is a subject of debate (Glover and Fritzsch, 2009). In pro-
tochordates, particularly urochordates, candidate placode- and
crest-like cells have been identified, and there is some expression
of placode- and crest-specific genes in both cephalochordates
and urochordates (Holland and Holland, 2001; Donoghue et al.,
2008; Hall, 2008; Holland et al., 2008; Schlosser, 2008; Glover and
Fritzsch, 2009; Yu, 2010; Graham and Shimeld, 2012). Recently,
Abitua et al. (2012) found the best candidate for a neural-crest
homologue in the pigment-for ming “A9.49” cells of tunicates,
but these cells do not mig rate nor form any ectomesenchyme as
true crest cells do. According to Glover and Fritzsch (2009), clear-
cut, definitive migratory neural crest appears to be absent from
cephalochordates and urochordates.
Whatever rudimentary precursors of placodes and neural crest
are in fact present in protochordates, the full development of these
structures marked a major transition in the evolution of the ner-
vous system. Indeed it has been proposed and largely accepted
that the neural crest and placodal systems represent the defin-
ing characteristics of the craniate line (Gans and Northcutt, 1983;
Northcutt and Gans, 1983; Northcutt, 1996a,b, 2005; Hall, 2008).
Kaas (2009) pointed out that the transformation of the neural
tube into a fully formed brain coincided with the establishment
of all the head’s special-sensory systems that are dependent on
the neural crest and placodes: image-forming eyes (via the lens),
the equilibrium-sensing ears, olfaction, taste and the lateral line
of fish.
But these correlated events need not have been exactly simul-
taneous. A recent study of gene expression (Sestak et al., 2013)
suggests that the placodes evolved slightly earlier than the neural
crest, or at least got a head start (also see Wada et al., 1998). The
evidence is that a good number of placode-associated genes are
expressed in developing tunicates (e ven though the adult placodal
derivatives are neither obvious nor vertebrate-like in tunicates),
but neural-crest-gene expression is high only in the vertebrates.
In summary, along with the evolutionary appearance of pla-
codes and neural crest came the enlarged brain of craniates, well
beyond that seen in the protochordates, with a complete crani-
ate forebrain, midbrain, and hindbrain. These brain structures
received and processed the input from the crest- and placode-
derived peripheral neurons for the senses of olfaction, taste,
equilibrium (and later, audition), and for the general somatic
senses of the head (Butler and Hodos, 2005). They provided the
central territory in which evolved isomorphic sensory maps and
images.
THE NEUROBIOLOGY AND PHYLOGENY OF NEURAL MAPS
AND SENSORY IMAGES
LAMPREYS AS THE M ODEL FOR EARLY SENSORY SYSTEMS
The lampreys and hagfish (jawless cyclostomes) are considered
the most basally arising extant members of the vertebrate clade.
Hagfish are secondarily specialized for a deep-ocean burrowing
lifestyle (Mallatt, 1997) so the free-swimming lamprey is generally
accepted as most closely resembling the first vertebrates in its sen-
sory and brain structures. This highly visual animal (Collin, 2009)
reveals that the camera-style eye was present by the time lampreys
and gnathostomes diverged over 460 million years ago (Mallatt,
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
1996; Lamb, 2011; Figure 1).Thesuccessofthevertebrateeye
stemmed from its innovations that contribute to the higher reso-
lution of a visual image, including a complex, spatially organized
three-layered retina; neural transmission from ciliary photorecep-
tors to chains of output neurons; enlargement of the eye allowed
by lateral ballooning of the optic vesicle from the wall of the
embr yonic diencephalon; the invagination of this ballooned vesi-
cle to form an eye cup; the addition of retinal computing power
in the form of retinal bipolar neurons, amacrine neurons, and
other interneurons; and the advent of the focusing lens, a placo-
dal derivative (Lamb et al., 2007, 2008; Lamb, 2011, 2013). Along
with its elaborate eye and lens, the lamprey has all the other ver-
tebrate features we have been emphasizing: the complete suite of
crest and placode derivatives, a well-developed peripheral ner-
vous system and trigeminal ganglia (Murakami and Watanabe,
2009), all the major elements of the tripartite brain (Figure 2C)
including a relatively large optic tectum in the mesencephalon,
a diencephalon with thalamus and hypothalamus, and a telen-
cephalon that contains an olfactory bulb and a small cerebral
hemisphere with a pallium (Nieuwenhuys, 1977; Iwahori et al.,
1987, 1999; de Arriba and Pombal, 2007; Fritzsch and Glover,
2009).
ORIGINAL ROLES OF TELENCEPHALON vs. TECTUM
Despite the existence of a telencephalon in lampreys and in the
reconstructed proto-vertebrate, there has been confusion over
how much of the highest-level sensory processing is/was per-
formed in the telencephalon vs. in the optic tectum of the
mesencephalon. The classical view was that at first the telen-
cephalon was only a “smell brain” while the tectum was the
“visual brain” (Wullimann and Vernier, 2009b). But by the 1970s
this view was refuted, largely because technical advances showed
the telencephalon of fishes and amphibians to be less olfaction-
dominated than was prev iously thought, and to contain all the
same non-olfactory structures as in “higher” vertebrates (e.g.,
the corpus striatum for selecting and maintaining behavioral
actions, the amygdala and other limbic structures for emotions,
and the hippocampus for forming memories) (Ebbesson, 1981;
Nieuwenhuys and Nicholson, 1998; Grillner et al., 2005; Jacobs,
2012; Kandel et al., 2012; Strausfeld and Hirth, 2013). However,
it is still likely that ancestrally, the telencephalon was where smell
input was processed and then integrated with information from
the other senses, especially in spatial memory-maps in the hip-
pocampal complex that allowed the animal to navigate through
space (Jacobs, 2012).
In birds and mammals, the telencephalic dorsal pallium per-
forms the highest-order processing of all senses based on isomor-
phic representations (Wild and Farabaugh, 1996; Wild et al., 1997;
Jarvis, 2009; Martinez-Garcia and Lanuza, 2009; Karten, 2013).
This pallial zone is especially dominant in mammals as the cere-
bral cortex (Kaas, 1983, 1997; Thivierge and Marcus, 2007). But
in the anamniotes including lampreys, the dorsal pallium lacks
this role (except in olfaction) and the optic tectum is the center of
sensory isomorphic representations. This claim is neither original
nor disputed but is widely accepted among fish and amphib-
ian researchers (Schuelert and Dicke, 2005; Binder et al., 2009;
Mueller, 2012). The tecta of non-mammalian vertebrates have
multiple isomorphic maps. The retinotopic maps closely overlap
auditory tonotopic maps, vestibular maps, lateral-line-receptive
maps, and somatosensory somatotopic maps (Sparks and Nelson,
1987; Sparks, 1988; Stein and Meredith, 1993; Hodos and Butler,
1997; Merker, 2007, 2012; Braun, 2009; Saidel, 2009; Cornide-
Petronio et al., 2011; Stephenson-Jones, 2012). Given this, we
deduce that the optic tectum, not the pallium, is the main site of
sensor y images and hence consciousness in anamniotes. Merker
(2005) deduced this from much the same evidence, and he also
emphasized the tectum’s laminar organization, which allows effi-
cient and extensive integration of the isomorphic input from the
different senses, and emphasized that the tectum receives multi-
system convergence from many other parts of the brain (de Arriba
and Pombal, 2007).
Additional support for the role of the anamniote tectum comes
from Dicke and Roth (2009) who stated, “In amphibians, as in
all anamniote vertebrates..., the tectum is the major brain cen-
ter for integrating visual perception and visuomotor functions. In
the amphibian tectum, localization and recognit ion of objects and
depth perception takes place. Three separate retino-tectal sub-
systems for object recognition exist, which process information
about (i) size and shape, (ii) velocity and movement pattern and
(iii) changes in ambient illumination. These kinds of information
are processed at the level of different retinal ganglion cells and
tectal neurons in close interaction with neurons in other visual
centers.” In this passage, we italicized the words that suggest visual
consciousness, which was also implied by Wullimann and Vernier
(2009a) when they said the fish tectum is for “object identifica-
tion and location,” and by Dudkin and Gruberg (2009) when they
said the tectum is for “discriminating between different classes
of objects, selecting (or attending to) one of several objects, and
directing movement of eye or head or body.” In describing the
role of the anamniote tectum in multimodal sensory processing,
Saidel (2009) said, “Among poikilothermic vertebrates, the tec-
tum has a coordinated map of space resulting from at least two if
not more senses that contribute to the transformation of synaptic
connections into a sensory map. The tectum might be considered
as a two-dimensional [grid] whose coordinate points, determined
from the visual field, both specify the external influences and per-
sonal space so that the appropriate action is spatially determined.
This would be the underlying basis of orientation behavior.”
Regarding the lack of any mammal-like isomorphic maps in
the telencephalic pallium of lower vertebrates, Wilczynski (2009)
wrote, “...all sensory systems not just olfaction reach large areas
of the telencephalon. In this general way, amphibians are similar
to other tetrapods, notwithstanding that the inputs are dominated
by a very heavy middle thalamic input to the striatum. The details
however, reveal a quite different functional organization from that
which might be expected... The telencephalic targets of ascending
sensory pathways are all multimodal. There is no evidence for sep-
arate representations for each sensory system, no indication of a
topographically preserved projection from any thalamic nucleus
to any telencephalic area and no physiological evidence for a sen-
sory (or for that matter motor) map. In esse nce, there is no e vidence
for the distinct, unimodal, mapped sensory representations that
are so prominent in the mammalian cortex. A possible exception
may be the core olfactory-recipient regions of the lateral pallium.
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
That is not to say that there is or is not a homologue of mam-
malian neocortex within the amphibian telecephalon, but there
are certainly no functional equivalents for the well-mapped, pure
sensor y zones that are so prominent in mammals and are signif-
icant telencephalic components in reptiles and birds” (emphasis
added). Though Wilczynski spoke of amphibians, this is also true
for the pallium of most fish (Wullimann and Vernier, 2009b;but
see Prechtl et al., 1998). But the lack of pallial isomorphism is even
more extreme in a few, exceptional, fish. For instance, in zebrafish
and goldfish of the carp family, neither the visual nor the auditory
sensory pathway seems to reach the dorsal pallium at all (Mueller,
2012). In conclusion, it is widely accepted that in anamniotes the
neurological basis for all sensory representations except olfaction
is within the optic tectum not the dorsal pallium.
IMPORTANCE OF VISION COMPARED TO THE OTHER SENSES
The importance of the visual tectum in lower vertebrates suggests
that visual representations were important in the earliest stages of
vertebrate evolution. All the sensory systems are remarkably con-
served across the vertebrates, and each resembles the visual system
in its basic organization (Shepherd, 1974; Pallas, 1990; Hodos
and Butler, 1997). Thus, the monopolar or pseudomonopolar
neurons of the olfactory, somatosensory, gustatory and auditory
receptors match the bipolar neurons that innervate the rods and
cones in the visual system in that all terminate on primary central
sensor y neurons called first order multi-polar neurons (Butler,
2000); and in most cases these first-order neurons project to the
optic tectum and the thalamus (Table 1). Furt her, Shepherd notes
that all the pr inciples involved in the formation of an initial visual
image in the retina, including “the initial image representation in
a two-dimensional sheet, lateral inhibition, temporal transients,
contrast enhancement, center-surround inhibition, and feature
extraction” (Shepherd, 2012, p. 65) also play essential roles in
the formation of neural “ images” in every other sensory system.
For example, in audition, individual nerve fibers from the ear
carry information that has an optimal sound frequency, and lat-
eral inhibition between fiber pathways sharpens the response to
that frequency. The same is true in the sense of touch, where tac-
tile discrimination depends upon the density of innervation of
the skin and lateral inhibition within central pathways (Shepherd,
2012).
Olfaction, however, shows some fundamental differences. Not
only is olfaction not processed by the midbrain tectum, but
also it is the only sense in vertebrates that reaches the pallium
and subpallium without an obligatory relay through the tha-
lamus (Gottfried, 2006, 2007; Shepherd, 2007, 2012; Ta b le 1).
Why the olfactory system does not require a thalamic relay is
an interesting question. Gottfried (2006) suggested it is because
the olfactory pathways evolved before the emergence of the tha-
lamotelencephalic pathways for the other senses. Whatever the
explanation, this fact underscores that a thalamic relay is not a
mandatory requirement for the presence of a conscious sensory
image (Shepherd, 2007, 2012).
The olfactory system of vertebrates forms an early smell
representation—which is comparable to a retinal visual
representation—at the level of the glomeruli within the o lfactory
bulb (Leon and Johnson, 2003; Gottfried, 2010; Shepherd, 2012).
From there, serial processing through the primary olfactory
cortex and then the orbitofrontal cortex forms a conscious smell
image (Tanabe et al., 1975; Zatorre and Jones-Gotman, 1991;
Gottfried, 2006, 2007; Shepherd, 2007; Li et al., 2010; Table 1 ).
The primary olfactory cortex is the highest unimodal region
in the olfactory pathway. Multimodal are the aforementioned
hippocampal maps (Jacobs, 2012) and the orbitofrontal cortex.
The latter is the main neocortical recipient of projections from
the olfactory cortex and has been posited to play a pivotal role
in olfactory associative consciousness (Li et al., 2010; Shepherd,
2012). It serves as an integration zone for olfactory afferents with
other sensory afferents (Price, 2007).
Although this description is based on mammalian studies,
lampreys and other anamniotes have homologous structures
throughout their olfactor y pathway: the olfactory bulb, then to
the “primary olfactory cortex” as their lateral pallium, which then
projects to the orbitofrontal-cortex homologue, namely to a part
of the dorsal pallium (Northcutt and Wicht, 1997; Wullimann
and Vernier, 2009b). From these similarities, we deduce that the
telencephalic pallium was a center of sensory (olfactory) con-
sciousness in early vertebrates, even though the optic tectum
dominated for the other conscious senses.
Nociception is an important sense to consider, given the cur-
rent scientific and popular interest in whether lower vertebrates
such as fish feel pain (Sneddon et al., 2003; Sneddon, 2004, 2011,
2012; Braithwaite, 2010). Nociception and pain are related phe-
nomena but are not identical. Nociception is a neurobiological
term that involves the neural processing of particular forms of
noxious stimuli that could cause tissue damage to the animal. The
International Association for the Study of Pain defines pain as
“an unpleasant sensory and emotional experience associated with
actual or potential tissue damage, or described in terms of such
damage” (Nordgreen et al., 2009; Sneddon, 2011). Nociception
may be reflexive, and only necessarily involves nociceptive neu-
ral pathways; pain is a psychological state, and entails sensory,
phenomenal consciousness (see Introduction). The most parsimo-
nious assumption is that the principles involved in the production
of “pain images” are the same as those involved in the pro-
duction of other sensory images such as visual images, auditory
images, etc.
While pain is a complex and multidimensional sensory experi-
ence based upon hierarchical somatosensory, affective, and home-
ostatic information processed in parallel and overlapping brain
networks (Craig, 2002, 2003a,b,c; Brooks et al., 2005), nocicep-
tors are actually quite ancient neural structures and are present
in species of molluscs, nematode worms, and fruit flies (Smith
and Lewin, 2009; Figure 4). In vertebrates, nociceptive neurons
with cell bodies in the dorsal root ganglia and innervating the
postcranial par t of the body are of neur al-crest origin, while those
innervating the face are in the trigeminal ganglia and der ive from
both neural crest and placodes (Fitzgerald, 2005; George et al.,
2007, 2010; Shiau et al., 2008).
While little is known about lampreys’ nociceptive abilities,
what is known suggests their nociception is primitive compared to
their other senses. The peripheral nervous system of the lamprey
has no myelinated nociceptive fibers, and recordings from spinal
and brain dorsal cells that have a potential nociceptive role have
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
FIGURE 4 | Various types of nociceptors found across different species. From Figure 4 in Smith and Lewin (2009) Springer. Reprinted with kind permission
from Springer Science+Business Media B.V.
achieved mixed results (Martin and Wickelgren, 1971; Rovainen
and Yan, 1985; Smith and Lewin, 2009). However, Matthews
and Wickelgren (1978) reported finding nociceptive neurons in
the lamprey trigeminal ganglia. Overall, these preliminary find-
ings suggest nociception is not robust in comparison to its other
sensory systems.
However, in the advanced bony fish (teleosts) such as trout,
zebrafish, carp, and perch, nociceptor fibers are comparatively
well-developed (Sneddon, 2003, 2004, 2011, 2012; Sneddon et al.,
2003; Nordgreen et al., 2009; Smith and Lewin, 2009; Braithwaite,
2010) and there is evidence for many of the structures thought
to be crucial for the central processing of pain (Figure 4). For
instance, in trout and goldfish, Dunlop and Laming (2005)
found that responses to both mechanoceptive (brush) and noci-
ceptive (pin-prod) stimuli ramified widely along the neuraxis
including the spinal cord, cerebellum, tectum, and telencephalon.
Trigeminal afferents in the hindbrain of goldfish show a clear pat-
tern of descending pathways and a topogr aphical organization
similar to that present in higher vertebrates (Puzdrowski, 1988).
Furthermore, in a host of teleosts, including trout, goldfish, and
zebrafish, there is solid behavioral evidence for sustained (in some
cases for hours), complex, and goal-directed responses to pain.
These responses include rubbing the skin at the site of an injection
of a noxious substance, reduction in typically ongoing behavior
such as feeding, avoidance of areas where painful stimuli were
administered, and inattention to competing stimuli (Sneddon,
2003, 2004, 2011, 2012; Dunlop and Laming, 2005; Ashley et al.,
2007; Millsopp and Laming, 2008; Reilly et al., 2008; Br aithwaite,
2010; Roques et al., 2010). Reilly et al. (2008) reported two of five
common carp r ubbed their lips against the tank walls after topical
injection of acetic acid into the lips.
Thus, the pain experience seems to characterize teleost fish
and presumably all other vertebrates with equally or more com-
plex brains (except perhaps for the cartilaginous fish such as
sharks, which may lack appreciable perception: Smith and Lewin,
2009; Sneddon, 2011). That is, the evidence suggests pain occurs
in the bony vertebrates that share the necessary neural crest-
and placode-derived nociceptors, the brain processing-centers,
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
and behaviors associated with pain processing. Teleosts may not
have the entire “pain hierarchy,” however, because the requi-
site sensory-somatotopy probably does not extend up to the
pallium (see above; Wilczynski, 2009). In contrast, in humans and
other primates, pain perception has a large cortical component,
and there are two candidate cortical regions for somatotopi-
cally mapped nociception—the primary somatosensory cortex
(SI) that emphasizes the exteroceptive aspects of pain perception
(Kenshalo et al., 2000; Mancini et al., 2012), and the insula, which
emphasizes its interoceptive aspects (Sherrington, 1906; Craig,
2002, 2003a,b,c, 2009, 2010; Price et al., 2003; Feinberg, 2009,
2011).
THE EVOLUTION OF IMAGE-FORMING EYES, THE CAMBRIAN
EXPLOSION, AND THE FIRST CONSCIOUS VERTEBRATES
In the timeline proposed by Lamb and co-workers (Lamb et al.,
2007, 2008; Lamb, 2011, 2013), beginning about 600 mya the
eye started to evolve from the simple frontal e ye characteristic
of cephalochordates into the vertebrate camera-style eye that was
fully developed by 500 mya and was similar to that of the mod-
ern day lamprey. This is also our view, although as mentioned,
we put the interval at 560–520 mya (Figure 1). The frontal eye of
larval amphioxus, limited to a few dozen cells, provides informa-
tion about the distribution of light and dark in the surroundings
and serves as a light and shadow detector, visual functions most
likely involved in establishing the animal’s orientation in the water
during feeding (Lacalli, 1996b, 2004). However, this lens-less eye
does not have the anatomy required for image-formation or com-
plex pattern-recognition; for example, for the detection of prey or
to guide complex locomotion (Lamb et al., 2007, 2008; Fernald,
2009; Lamb, 2011).
Attaining image-forming eyes had profound implications for
the evolution of animal groups. According to the “Light Switch”
hypothesis proposed by Parker (2003), the nearly simultane-
ous appearance of image-forming eyes in numerous phyla led
directly to the diversification of the bilaterian animals during the
Cambrian explosion approximately 541 million years ago. In this
account, pre-Cambrian animals possessed primitive chemorecep-
tors and simple light receptors as exist in amphioxus, but it was
the evolution of image-forming eyes that led to the explosive
improvements in directed locomotion and food seeking, food
handling, predation and avoidance of predators, and the ori-
gin of hard body parts as defense against predators. Trestman
(2013) recently fleshed out the Lig h t Switch hypothesis by detail-
ing how the appearance of object-oriented, spatial vision led not
only to brain elaboration but also to a basic kind of “cogni-
tion” that controlled the body actions of locomotion and feeding.
Further buttressing the Light Switch and vision-first hypothesis,
many new retina-associated genes seem to have been added in the
earliest Bilateria and their immediate descendants (Sestak et al.,
2013).
The centrality of vision in the evolution of the vertebrate brain
finds support from studies of embryonic development and cel-
lular differentiation. For instance, although the fates of placodal
structures are varied, and the y contribute to multiple special sen-
sory structures including the eye lens, inner ear and olfactory
epithelium, Baile y and co-workers (2006) foundthatinthechick
embryo, the entire preplacodal region is initially specified as lens
tissue, a finding that implies that “lens” is the default state of the
preplacodal territory and that all the non-lens placodal deriva-
tives, such as those contr ibuting to the inner ear, evolved later.
In her intriguing scenario of the evolution of vision and
thebrain,Butler(Butler, 2000, 2006; Butler and Hodos, 2005)
hypothesized how the advent of an advanced visual system
played an early and critical role in the formation of the ver-
tebrate brain. She proposed that there was a transitional ani-
mal between a cephalochordate-like ancestor and the first true
craniates, which she called a “cephalate” (a combination of
the words “cephalochordate” and “craniates”). This hypothetical
creature (Figure 5A) had paired eyes and a fairly well-established
diencephalon- and mesencephalon-based visual system (note that
the vertebrate retina is embryologically a direct outgrowth of the
diencephalon), but at this early stage it lacked most of the contri-
butions from neural crest and placodes, and lacked a craniate-
type peripheral nervous system and a definitive telencephalon.
According to this account, the transition from cephalochordate
to craniate was sequential, beginning with the establishment of
paired, lateral eyes and optic nerves followed by elaboration of
the descending visual pathway to brainstem motor centers. These
visual pathways served as a circuitry template for the subsequent
arrival of the new sensory systems, both ascending and descend-
ing, that evolved with the advent of the neural crest and pla-
codes including the somatosensor y, olfactory, otic-equilibrium,
and gustatory systems. She argued that this model explains the
marked uniformity of the pattern across the different central-
sensory pathways of vertebrates (Tabl e 1 ). Butler’s hypothesis
suggests to us that the appearance of the visual image was the ear-
liest manifestation of sensory consciousness, followed by others.
This eye-first view could be questioned. For example, Plotnick
et al. (2010) reasoned that olfaction evolved first, on mostly
theoretical-ecological grounds. But the actual evidence favors
FIGURE 5 | Nervous systems of pre-vertebrates. (A) The “cephalate” as
hypothesized by Butler (2000, 2006; Butler and Hodos, 2005). (B)
Haikouella. This fossil animal is interpreted to have had paired eyes, less
prominent or absent olfactory organs, a poorly developed telencephalon,
and no otic or vestibular organs (Mallatt and Chen, 2003; Chen, 2009,
2012). Mallatt and Chen (2003) propose that Haikouella supports Butler’s
model of the hypothetical cephalate.
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
eye-first. Sestak et al. (2013) found that the surge of newly evolved
retina- and lens-associated genes pre-dated that of new olfac-
tory, otic, and lateral-line genes, having occurred before, vs. after,
the appearance of the “tunicate + vertebrate” line of animals.
Additionally, Vopalensky et al. (2012) used gene-expression pat-
terns to show that larval amphioxus has photoreceptors, pigment
cells, and projection neurons that are homologous to those in the
retina of vertebrates, yet amphioxus lacks vertebrate-like olfactory
and equilibrium sensors. Third, fossil pre-vertebrates show more
evidence of eyes than of olfactory organs, as we will now discuss.
Evidently supporting the cephalate model are the fishlike, fos-
sil y unnanozoans, from the Yunnan Province of China, of which
Haikouella lanceolatum (Figure 5B) is known in the most detail
(Chen et al., 1999; Chen and Li, 2000; Mallatt and Chen, 2003;
Mallatt et al., 2003). Haikouella dates from the Early Cambrian
520 mya, not long after the hypothesized emergence of visual pre-
vertebrates at 560–520 mya. Haikouella was 25–30 mm long and
possessed a notochord, paired eyes, a prominent hindbrain, and
a diencephalon located in the same positions as are these struc-
tures in extant vertebrates such as the lamprey. As interpreted by
Mallatt and Chen (2003), Haikouella had no skull or ears, and it
had at most a weakly developed telencephalon. This brain region
may require a fully developed olfactory placode for its induction
(Butler, 2000, 2006; Butler and Hodos, 2005), which would imply
that Haikouella had only a tiny or non-existent olfactory placode;
indeed, only hints of olfactory capsules and nostrils are seen in
the adult fossils. Thus, Haikouella, despite having the vertebrate
eyes, appears to have lacked many of the skeletal and peripheral-
nervous components that are present in vertebrates with fully
evolved neurogenic placodes and neural crest.
But Haikouella had gill bars, which are neural-crest derivatives,
and in the center of each eye, a dot-like lens, which is a placode
derivative (Figure 7 in Mallatt and Chen, 2003). With its e yes, pla-
codes and neural crest, and a brain whose overall size matches that
of modern vertebrates (i.e., lampreys), Haikouella is a candidate
for the earliest conscious organism on earth, or at least the earliest
conscious chordate.
It should be noted, however, that the interpretation of the
Haikouella fossils is not without controversy. Most prominently,
Shu and co-workers have questioned Haikouella’s evolutionary
placement and even the existence of eyes, a notochord, or a
brain in this animal (Shu et al., 1996, 2009; Shu, 2003;alsosee
Donoghue and Purnell, 2009). This leaves another 520-million-
year-old group from the same fossil beds, Haikouichthys ercai-
cunensis (Figure 6) and related species, as best indicating the early
evolution of the vertebrate nervous system (Shu et al., 1999, 2003,
2009; Hou et al., 2002; Shu, 2003; Chen, 2012).
Haikouichthys is widely agreed to have been a true verte-
brate, a jawless fish, and it shows vertebral elements, promi-
nent eyes, and otic and olfactory capsules, although no trace
of Haikouichthys’ brain has been preserved in the fossils. As
avertebrate,Haikouichthys would be a more evolved species
than Haikouella (Chen, 2012) and is therefore possibly less
informative about the features of a putative transitional pre-
craniate. Nonetheless, whichever of these fossil groups represents
the progenitor of craniates (or is an early craniate), the paired eyes
of Haikouella,otheryunnanozoans,andHaikouichthys ranged in
FIGURE 6 | Haikouichthys.(A)Artist’s rendering of what Haikouichthys
looked like. (B) Fossil of this animal with an eye and otic capsule (“Auditory
vesicle”) labeled. Haikouichthys is agreed to have been a true vertebrate, a
jawless fish, and it shows vertebral elements (protovertebrae), prominent
eyes, and nasal capsules (Shu, 2003; Shu et al., 2003, 2009). From Figure
146 in Chen (2012) Springer. Reprinted with kind permission from Springer
Science+Business Media B.V.
size from 0.2 to 0.6 mm in diameter, and thus were considerably
larger than the frontal eye of amphioxus, which is only 10 microns
in diameter. This suggests that the eyes of these fossil animals
had more neuronal layers, forming two-dimensional receptor
fields that produced retinal images, at least in the larger-eyed
Haikouichthys (Chen, 2012). Based upon our aforementioned
criteria, Haikouichthys possessed primary consciousness.
THE SIMPLEST EXTANT VERTEBRATES WITH
CONSCIOUSNESS: THE ARGUMENT FOR THE LAMPREY
In our hypothesis, the creation of a sensory neural map requires at
a minimum a brain and t ypical neurohierarchical structure, with
consciousness emerging from progressively more complex and
integrated patterns of isomorphic organization in the upper lev-
els of this hierarchy (Ta b l e s 1, 2; Feinberg, 2009, 2011, 2012). But
the brain-maps for the different senses are not isolated from one
another. They are integrated in two critical ways. First, the highest
levels are multimodal; for example, the visual, auditory, vestibu-
lar, and somatosensory maps all stack in register in the midbrain
tectum (Guirado and Davila, 2009; Saidel, 2009); as another
example of this, extensive multimodal association-areas and asso-
ciation fibers interlink the different primary sensory-areas in the
cerebral cortex of mammals (Mesulam, 2000; Feinberg, 2011).
The second critical feature of the neural correlates of con-
sciousness is widespread interaction among such separate brain
regions as the reticular-activating system (RAS) of the reticu-
lar formation, the thalamus, and the optic tectum or cerebral
pallium/cortex, as these brain regions receive and integrate sen-
sory representations into neural networks that contribute to
attention, awareness, and neural synchronization (Penfield, 1975;
Baars, 1988, 2002; Edelman, 1989, 1992; Newman and Baars,
1993; Crick, 1994; Llinas and Ribary, 2001; Ribary, 2005; Seth
et al., 2005; Min, 2010; Edelman et al., 2011). Therefore, for a
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
Table 2 | Neural features, functions, and genes proposed to contribute to consciousness in vertebrates.
Feature Function Genes involved References
Paired lateral eyes Gather visual images, guide vision-related
actions. Retinas of these eyes develop
from the diencephalon and co-evolve with
a tripartite brain
Pax4/6 (etc.) Shu et al., 1999, 2003, 2009; Butler,
2000; Collin et al., 2003*; Vopalensky
et al., 2012; Lamb, 2013
Fully differentiated
tripartite brain
Provides for a sensory-neural hierarchy up
to pallium or cerebral cortex (amniotes), or
to optic tectum and thalamus (anamniotes)
Emx (dorsal pallium)
Otx2, Fgf8, En,etc.(tectum)
Friedman and O’Leary, 1996;
Nieuwenhuys and Nicholson, 1998*;
Butler, 2000, 2006; Murakami and
Kuratani, 2008*; Rhinn et al., 2009;
Sprecher, 2009
Placodes and
neural crest
Provide lens of eye and the lower levels of
the neural hierarchies of all major
isomorphic sensory systems in
vertebrates, except the visual
Holland and Holland, 2001; McCauley
and Bronner-Fraser, 2002*, 2003*;
Baker, 2005; Schlosser, 2005, 2008,
2010; Donoghue et al., 2008; Hall, 2008,
2009; Graham and Shimeld, 2012
Placode genetics Six1, Six4, Eya (all placodes), Robo2
(trigeminal ganglion), Pax genes
including Pax6 (lens)
McCauley and Bronner-Fraser, 2002*;
Bailey et al., 2006; Schlosser, 2008;
Shiau et al., 2008; Yu, 2010
Neural crest
genetics
Snail1/2, FoxD3, Twist, Hoxb2, Hoxa2,
Hoxb3, Hoxa3, Slit1
Trainor and Krumlauf, 2000; Murakami
and Kuratani, 2008*; Schlosser, 2008;
Shiau et al., 2008; Yu, 2010
Reticular
activating system
(RAS)
Widespread brain activation mediating
attention and arousal
Moruzzi and Magoun, 1949; Parvizi and
Damasio, 2001; Dehaene et al., 2003;
Manger, 2009
Reciprocal
tecto-thalamic
interactions
Proposed integration of higher order
sensory representations
Heier, 1948*; Nieuwenhuys and
Nicholson, 1998*; Merker, 2005, 2007
Isomorphic neural
representations
Provide for the spatial or non-spatial
mapping of the external or internal
environment
Hamdani and Doving, 2007*; Murakami
and Kuratani, 2008*; Cornide-Petronio
et al., 2011*; Kandel et al., 2012;
Stephenson-Jones, 2012*
Isomorphic
genetics
Hoxa2, EphrinA, EphrinB, Tnc, Nov,
Slo, En-1, En-2
Friedman and O’Leary, 1996;
McLaughlin and O’Leary, 2005; Gosse
et al., 2008; Murakami and Kuratani,
2008*; Bevins et al., 2011; Frucht et al.,
2011; Son et al., 2012
Color vision Provides for the phenomenal/subjective
representation of different
light-wavelengths
Opsins Jacobs, 2009; Lamb, 2013*
Non-visual sense
organs (olfaction,
taste,
somatosensory,
equilibrium and
hearing, lateral
line,
electroreception)
Various chemosensory, mechanosensory,
and electrosensory functions.
Well-developed olfactory sense can guide
complex food-finding and migratory
patterns
OR, TAAR, V1R (olfactory), TR,
PKD2L1 (taste), various ion-channel
genes (hearing, equilibrium, touch,
pain)
Braun and Northcutt, 1998*; Vrieze and
Sorensen, 2001*; Shu, 2003*; Shu et al.,
2003*; Chung-Davidson et al., 2004*;
Chandrashekar et al., 2006; Libants
et al., 2009*; Niimura, 2009; Vrieze
et al., 2010*; de Brito Sanchez and
Giurfa, 2011; Horwitz et al., 2011;
Kawashima et al., 2011; Geffeney and
Goodman, 2012; Roudaut et al., 2012;
Baker et al., 2013
Asterisks (
*
) indicate the references that specifically document the features in lampreys and other fish.
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
cyclostome brain to create sensory mental images, its isomor-
phic representations must be integrated into this wider neur al
network. In fact, there is ample evidence that the most studied
cyclostome nervous system of the lamprey satisfies this second
requirement (Nieuwenhuys, 1972, 1977; Polenova and Vesselkin,
1993; Northcutt and Wicht, 1997; Nieuwenhuys and Nicholson,
1998), as will now be elucidated.
The lamprey nervous system possesses every typical sensory-
integration center of vertebrates including the optic tectum, the
dorsal thalamus, the RAS in the tegmentum, the telencephalic
pallium and olfactory bulb (Figure 7)(Heier, 1948; Wicht, 1996;
Nieuwenhuys and Nicholson, 1998). The lamprey brain also has
the widespread interactions and neurohierarchical properties that
we consider necessary for sensory consciousness. Let us examine
the integration centers one by one.
We already mentioned the optum tectum’s role in sensory inte-
gration and isomorphic-map formation in the lamprey (Saidel,
2009; Stephenson-Jones, 2012), which would make it the key con-
tributor to all non-olfactory sensory consciousness. To expand
FIGURE 7 | Brain regions in lampreys, emphasizing the connections of
the dorsal thalamus (DT) according to Nieuwenhuys (1972);
Nieuwenhuys (1977) and Nieuwenhuys and Nicholson (1998).(A)
Afferents to dorsal thalamus. (B) Efferents from dorsal thalamus. II, optic
nerve; Bol, olfactory bulb; CP, commissura posterior; Hab, ganglion
habenulae; LS, lobus subhippocampalis; ML, medial lemniscus; NDH,
nucleus dorsalis hypothalami; NVH, nucleus ventralis hypothalami; NTP,
nucleus tuberculi posterioris; PinOrg, pineal organ; PHip, primordium
hippocampi (= hippocampus, medial pallium); PR, nucleus preopticus; Str,
corpus striatum; PT, area pretectalis; Tect, tectum mesencephali; Teg,
tegmentum; TSC, torus semicircularis.
on this consideration of the tectum in consciousness, the nearby
isthmus nucleus has now been identified in lampreys (Robertson
et al., 2006). The isthmus nucleus signals the tectum to direct
attention to important objects in the v isual field (in birds, see
Wylie et al., 2009), or at least it arouses and alerts the system
that something is mov ing in the field (in teleosts: Dudkin and
Gruberg, 2009). Either of these roles could be a part of conscious
perception.
Turning to the dorsal thalamus of lampreys (Figure 7), Heier
(1948) and Nieuwenhuys and Nicholson (1998) concluded this
is another higher-order integration center for correlating various
types of afferent information. That is, it integrates informa-
tion from the tectum (vision and most other senses), olfactory
bulb (smell), and the spinal cord and rhombencephalon (the
somatosensory information carried by the spinothalamic tracts
and trigeminal nuclei). In this way, the thalamus would interact
with the tectum to help generate tectal consciousness. This simple
idea is similar to Merker’s (2005, 2007) more complex interpre-
tation, but without the latter’s radical claim that the center of
consciousness in mammals is the brainstem instead of the cerebral
cortex (cf. Crick, 1994; Fries et al., 1997; Zeki and Marini, 1998).
Along with its tectal interactions, the dorsal thalamus of verte-
brates is the station for reciprocal communications between the
telencephalon and the rest of the brain (Butler, 2008b). As in
other vertebrates, the lamprey’s dorsal thalamus projects to the
cerebral pallium (Figure 7B) indicating a pallial role in sensory
processing (Polenova and Vesselkin, 1993; Northcutt and Wicht,
1997).
Additionally, the lamprey brain possesses a well-developed
reticular formation with extensive reciprocal connections to the
dorsal and ventral thalamus, the latter actually including the
most rostral part of the reticular formation (Stefanelli, 1934;
Heier, 1948; Nieuwenhuys and Nicholson, 1998; Butler, 2008b).
In all vertebrates, the reticular formation signals widespread
activation of the cerebrum and thus is required for alertness,
awareness, attention, and consciousness (Moruzzi and Magoun,
1949; Parvizi and Damasio, 2001; Dehaene et al., 2003; Manger,
2009). In lampreys and other anamniotes, this RAS could acti-
vate the tecto-thalamic sensory consciousness that we have pro-
posed. In mammals, the system is elaborated into a reticular
formation-thalamocortical complex that is essential for mam-
mals’ cerebrum-dominated consciousness (Baars, 1988, 2002;
Edelman, 1989, 1992; Newman and Baars, 1993; Crick, 1994;
Llinas and Ribary, 2001; Ribary, 2005; Schiff, 2008; Seth et al.,
2005; Min, 2010; Edelman et al., 2011). In the anamniotes,
such a reticular-thalamocortical complex has been proposed
but never verified experimentally (Butler, 2008b). If present,
it must be smaller, given the small size of the cerebral-cortex
homologue (dorsal pallium) of lampreys and most other anam-
niotes (Murakami e t al., 2001; Muhlenbrock-Lenter et al., 2009;
Wullimann and Vernier, 2009b).
Some theories of primary consciousness, particularly those of
Edelman (1989, 1992; Edelman et al., 2011), implicate memory
functions as a key component. Memory construction in verte-
brates is performed by the hippocampus (Martin et al., 2000;
Jacobs, 2012). Although functional investigations are lacking for
lampreys, their telencephalon does possess a hippocampus or
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
medial pallium (Nieuwenhuys, 1977; Polenova and Vesselkin,
1993; Northcutt and Wicht, 1997; Nieuwenhuys and Nicholson,
1998). The lamprey hippocampus (PHip, s ee Figure 7) has the
typical, widespread, connections within the brain, including to
the dorsal thalamus, the optic tectum, dorsal pallium, and the
olfactory bulb.
The neurohierarchical pathways for all major senses have been
documented in lampreys, as summarized by Nieuwenhuys and
Nicholson (1998). They are widely recognized to be very simi-
lar to those of other vertebrates, especially of other anamniotes
(Binder et al., 2009).
In summary, the lamprey brain possesses all the requisite
regions and neurohierarchical pathways for visual, olfactory,
somatosensory and other images, integrated together to produce
attention, awareness, neural synchronization and memory—all
the elements proposed to be necessary for conscious awareness.
Thus, given our assumptions of the sufficient neural underpin-
nings, we conclude that the lamprey has at a minimum sensory
consciousness.
GENES AND CONSCIOUSNESS
Consciousness may now be understandable from an entirely new
perspective, that of genetics. Murakami and Kuratani (2008)
found developmental-genetic evidence for our proposal that
somatotopy and consciousness emerged during the transition
from cephalochordate-like ancestors to vertebrates. They found in
lampreys that the trigeminal sensory neurons project somatotopi-
cally to the relay nuclei in the hindbrain, with the neurons of these
brain nuclei being organized in the same somatotopic pattern as
in the t rigeminal nerve. This somatotopic relationship also occurs
in all gnathostome vertebrates, where the connections and nuclei
are patterned by expression of Hoxa2, a genetic-transcription
factor that also patterns the developing hindbrain into bulged seg-
ments called rhombomeres. Significantly, Murakami and Kuratani
demonstrated this same association of somatotopy, Hoxa2, and
rhombomeres in the lamprey. Thus, they tied one key compo-
nent of consciousness, isomorphic somatotopy, to a specific gene,
Hoxa2.
Second, Hox-gene expression in the rhombomeres, including
expression of Hoxa2, is known to signal the patterning of neural
crest in the vertebrate head (Trainor and Krumlauf, 2000), includ-
ing signaling the crest-derived sensory neurons that are unique to
vertebrates and are located at the start of the conscious-sensory
pathway. In fact, the extensive gene networks involved in the
development of neural crest and ectodermal placodes have been
worked out in considerable detail (networks with Snail1/2, FoxD3,
Twist, Six1, Six4, Eya, and many more genes; Sauka-Spengler and
Bronner-Fraser, 2008; Schlosser, 2008; Shiau et al., 2008; Yu, 2010;
Grocott et al., 2012). Thus, a second aspect of consciousness as we
have proposed it, namely the neural crest- and placode-derived
neurostructure, is tied to multiple, specific genes.
Third, genetic signals have been identified for the development
of retinotopy in the brain (En-1 and En-2 signals: Friedman and
O’Leary, 1996; EphrinA signals: Gosse et al., 2008; B evins et al.,
2011), as have genes in the ear related to tonotopy (Tnc, Nov,
Slo: Frucht et al., 2011; Son et al., 2012). These pathways have
been found in zebrafish, birds, and mammals, but have not been
investigated in lampreys. Still, they show retinotopy and tonotopy
to be two more aspects of proposed consciousness that are tied to
specific genes.
In embryonic vertebrates, the dorsal pallium (likely critical for
consciousness in mammals and birds) is characterized by expres-
sion of the Emx transcr iption factor. Emx is also expressed by
the dorsal pallium of lamprey embryos (Murakami et al., 2001),
although we reiterate that, except for olfaction, this region is not
involved with isomorphic sensory consciousness in anamniotes
(Wilczynski, 2009). Nonetheless, the fact remains that all groups
of vertebrates express the Emx gene that has been associated with
consciousness in mammals and birds; this ties another gene to
consciousness. As for the optic tectum, which we associate with
consciousness in anamniotes, key genes that signal its develop-
ment are also known (Otx, Fgf8, En,andothers:Friedman and
O’Leary, 1996; Butler, 2000; Murakami et al., 2001; Rhinn et al.,
2009; Sprecher, 2009).
By contrast, the non-vertebrate amphioxus has none of the
structures that we associate with consciousness in vertebrates.
It has no crest/placode-derived trigeminal or spinal sensory
neurons, no Hoxa2-specified rhombomere segments (although it
does express Hox2 in an unsegmented strip in its hindbrain), and
it has no tectum, tectum genes, or telencephalic pallium (Wicht
and Lacalli, 2005; Murakami and Kuratani, 2008; Schlosser, 2008;
Yu, 2010; Pani et al., 2012; Figure 2A).
In summary, the genetic data support the existence of a hier-
archy of somatotopy in lampreys that is based on the same gene
suite as in mammals and other gnathostomes, and which evolved
after the divergence from amphioxus ( see the timeline in Figure 4
of Murakami and Kuratani, 2008). Thus, these genes could be a
proxy for the appearance of consciousness at the start of the ver-
tebrate line, the same timing we proposed based on other lines of
evidence. Additional genes, which we associated with the retino-
topic and tonotopic aspects of consciousness in vertebrates, also
support this conclusion. Many of the genes are fully characterized
down to their DNA sequences in multiple groups of vertebrates
(e.g., the Hox genes: Takio et al., 2004). By our hypothesis, con-
sciousness is in our genes, and some of these genes have been
identified.
Table 2 lists all the neural features we have associated with
consciousness in vertebrates, with genes that contribute to these
features. It includes not only the genes we considered here in the
text but also s ome other genes that are expressed in the receptors
at the start of the sensory pathways.
DISCUSSION
RECAP AND EVOLUTIONARY SHIFTS IN SENSORY CONSCIOUSNESS
Using multi-level, isomorphic sensory representations in ver-
tebrates as a “marker” for the presence of sensory images
and hence phenomenal, primary consciousness, the minimum
requirement for such consciousness in chordates is a tripartite
brain including a craniate forebrain (but not necessarily a highly
developed dorsal pallium), a midbrain, and a hindbrain. We rea-
soned that t his brain must feature: (1) a hierarchical system of
isomorphically organized, reciprocally communicating, sensory-
integration nuclei and centers, with conscious images emerging
from the higher-level processing of different sensory modalities
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
and submodalities (Ta b le 1); and (2) interactions among the RAS,
thalamus, and tectum or pallium that integrate sensory represen-
tations into a wide neural network that contributes to arousal
and thereby to consciousness (Baars, 1988, 2002; Edelman, 1989,
1992; Newman and Baars, 1993; Crick, 1994; Llinas and Ribar y ,
2001; Ribary, 2005; Seth et al., 2005; Min, 2010; Edelman et al.,
2011). By this reasoning, the cephalochordates and tunicates are
not conscious because they lack the key features. But the lam-
prey, representing the most basal of the living vertebrates, has
all these features and thus is hypothesized to possess sensory
consciousness.
We suggest that during vertebrate history, the neural center of
primary consciousness changed in two major steps. Multimodal
and isomorphic sensory consciousness first evolved around the
visual sense and thus initially centered in the visual tectum of
the midbrain, although olfactory perception involved the telen-
cephalic pallium (step 1: fish and amphibians). Direct evidence of
eyes and indirect evidence of a tripartate brain, neural crest, and
placodes occur in fossils from the Early Cambrian. From this we
deduce that sensory consciousness arose at least 520 million years
ago, and was a primary driver of vertebrate evolution because
its participation is required for complex animals to exploit novel
habitats by more effectively sensing the environment. Table 3 pro-
vides an evolutionary timeline for the emergence of consciousness
in this first step.
Next, in a second major step, in ancient amniotes of the
pre-mammal and sauropsid-reptile lineages, the dorsal pallium
gradually became the dominant center of sensory consciousness,
mostly independently in the two lineages (step 2: amniotes). The
mammalian step culminated when true mammals evolved from
mammal-like reptiles in the late Tr iassic (about 200 mya), and
the sauropsid step somewhat later, in the first birds (around 180
mya). Actually, the step was probably gradual in both these lines
of amniotes, its full duration spanning the Late Paleozoic and
Early Mesozoic from roughly 350–180 million years ago (Benton
and Donoghue, 2007). In the earliest mammals, this step to pallial
consciousness can be related to a shift from vision to olfaction as
the dominant sense (Rowe et al., 2011), but no such sensory shift
occurred in the evolution of birds, where olfaction even declined
(Roper, 1999). This inconsistency makes the change to pallial con-
sciousness in birds difficult to explain. Still, one can speculate
for both birds and mammals that when the center of sensory
consciousness shifted from the optic tectum to the markedly
enlarging and increasingly complex dorsal pallium, it involved an
expansion and enrichment of the conscious experience.
The second step in mammals merits further consideration. It
nicely shows that a lthough brains became more complex dur-
ing the half-billion year saga of vertebrate evolution, not all of
the sensory systems did. The visual system of the early, noctur-
nal, mammals was regressed compared to that of their diurnal,
highly visual reptilian ancestors (Bowmaker, 1998; Jacobs, 2009;
Hall et al., 2012), and the proto-mammalian olfactory system
was highly developed for a keen sense of smell (Rowe et al.,
2011). Regression in vision probably explains why the tectum
of mammals (superior colliculus) is less elaborate than that of
extant reptiles and birds, who retained acute vision throughout
their entire history (Aboitiz, 1992). When most orders of early
mammals became diurnal again, probably after the extinction of
the dinosaurs, vision became more important and the retina and
visual areas of the cerebral cortex expanded in size and complex-
ity. This especially occurred in the keen-sighted primates, where
the regions for olfactory processing were reduced (Allman, 1999).
With these back-and-forth shifts in the dominant sense dur-
ing mammalian evolution, the central hub of sensory-conscious
experience shifted between the olfactory and visual cortex.
Additionally, different sensory systems became highly elabo-
rate or regressed in other lines of vertebrates. One example is
the extreme development of electroreception in some teleosts
(“electric fish”) with enlargement of the processing part of their
cerebellum and cerebral pallium (Prechtl et al., 1998; Wullimann
and Vernier, 2009a). Another, more dramatic example is the
sister cyclostome of the lamprey, the hagfish, whose nervous sys-
tem and proposed consciousness were shaped by their unusual
lifestyle of burrowing in soft sediment of the dark ocean floor
(Mallatt, 1997). Hagfish have a regressed visual system, a rudi-
mentary lateral line, and perhaps a simplified inner ear, but
they enjoy highly sensitive olfaction, exaggerated touch percep-
tion, and abundant taste-like chemoreceptors in the skin of their
head (Andres, 1993; Braun, 1996; Braun and Northcutt, 1998;
Von During and Andres, 1998; Lamb, 2013), all of which help
them to locate and feed upon carcasses on the ocean bottom
and to prey on live worms and burrowed fish within the sedi-
ment (Zintzen et al., 2011). Along with these “extreme senses,”
the hagfish has a large, well-developed brain (Wicht, 1996; Ronan
and Northcutt, 1998; Wicht and Nieuwenhuys, 1998; Wicht and
Northcutt, 1998). This brain features all the major sensorimo-
tor systems with the exception of an oculomotor system, and
has especially robust olfactory and trigeminal-sensory represen-
tations. What is it like to be a hagfish? Any conscious experience
would center on three-dimensional mental “images” of richly per-
ceived and spatially discriminated smells, touch sensations, and
taste stimuli, all in virtual blindness.
OBJECTIONS TO THE HYPOTHESIS
Challenge 1: Isomorphism does not equal consciousness
Our thesis could be challenged in four ways. First, one might
argue that isomorphic representation cannot be equated with
consciousness because artificial sensors and computers can
receive and map out stimuli, yet these machines are not con-
scious. In response, we reiterate that our hypothesis states that
sensor y consciousness and isomorphic representations entail a
highly specific “kind” of isomorphic representation, not just any
kind. The brain possesses an entirely unique architecture that
features—in addition to a huge “computer-like” amount of com-
plex processing—reciprocal communication between the levels of
the neural hierarchy with integrated and novel emergent proper-
ties appearing with the addition of each level. Thus, the neural
hierarchy represents a unique neurobiological substra te and orga-
nization quite different from that found in computers made of
silicon chips and wires (Feinberg, 2012).
Challenge 2: Consciousness is “corticothalamic” and should be
studied from the top down
The second challenge says it is better to search for non-human
consciousness by starting with entities known to be conscious.
That is, beg in with humans and the animals most closely related
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
Table 3 | Timeline of the emergence of critical features of sensory consciousness in vertebrates.
Feature/Taxon Timeframe
1
(million years ago)
Earliest fossil evidence
(animal fossils)
References
Ediacaran period 635–541 Sponges Erwin et al., 2011; Erwin and Valentine, 2013
Cambrian period 541–488 Worm trace: Treptichnus
pedum
Peterson et al., 2008; Erwin and Valentine,
2013
1. First chordate 560–520 No direct fossil evidence See Figure 1, based on earliest body fossils of
any bilaterian animals being about 560 my old
(Erwin and Valentine, 2013)
2. Common ancestor of tunicates
and vertebrates (and first
precursors of placodes?)
560–520 Shankouclava (fossil
tunicate)
See Figure 1; Chen et al., 2003; Sestak et al.,
2013
3. Paired lateral eyes 560–520 Haikouichthys Shu et al., 1999, 2003, 2009; Butler, 200 0;
Vopalensky et al., 2012
4. Fully differentiated tri-partite
brain
2
560–520 (460) Haikouella, or the first
gnathostome-fish fossils
2
Janvier, 1996; Butler, 2000, 2006; Mallatt and
Chen, 2003; Murakami and Kuratani, 2008;
Sprecher, 2009
4. Cephalate animal 560–520 Hypothetical, so no fossil
evidence
Butler, 2000, 2006
5. Placodes and neural crest 560–520 Haikouella and
Haikouichthyes
Shu et al., 1999, 2003, 2009; Mallatt and Chen,
2003; Hall and Gillis, 2013
5. Isomorphic neural
representations
2
560–520 (460) Murakami and Kuratani, 2008;
Stephenson-Jones, 2012
5. Non-visual sense organs-1
(olfaction, trigeminal
somatosensory)
560–520 Haikouichthys (and
Haikouella?)
Mallatt and Chen, 2003; Shu, 2003; Shu et al.,
2003
5. Sister group of vertebrates:
Haikouella
520 Yunnanozoans Chen et al., 1999; Chen, 2012
6. Non-visual sense organs-2
(equilibrium, taste? lateral line?)
2
560–520 (460) Haikouichthys, Astraspis,
and Sacabambaspis
Sansom et al., 1997; Braun and Northcutt,
1998; Shu, 2003; Shu et al., 2003
7. Vertebrate: Haikouichthys 520 Haikouichthys and related
genera
Shu et al., 1999, 2003, 2009
Note the near-simultaneity of appearance of all features, near the time of vertebrate origin.
Features and taxa are numbered as 1–7 in the estimated order of their evolutionary appearance. Repeated numbers mean the different events occurred together or
nearly simultaneously.
1
Dates of the features are taken from the fossil record (see text).
2
These features are not directly observable in the 520 million-year-old Haikouichthys fossils, but are inferred to have existed in that vertebrate because some
correlated structures did. Conceivably, the feature might date to as late as the cyclostome (agnathan)-gnathostome split at 460 mya (Mallatt, 1996), but no later
because both lampreys and gnathostomes have it.
to us, namely apes and the other mammals and then search care-
fully, using homology and analogy, for signs of consciousness
in slightly simpler brains such as those of reptiles. Most stud-
ies of comparative animal-consciousness proceed this way (e.g.,
Edelman et al., 2005; Butler, 2008a; Mashour and Alkire, 2013).
This is preferable, it could be said, to our seeking consciousness
in the distantly related lower-vertebrates like lampreys, where any
version of consciousness could be strange or absent and therefore
harder to recognize, to prove, or to disprove. The human-first
approach is top-down, whereas ours is bottom up.
A potential weakness of our bottom-up approach—searching
for consciousness in the simplest animals that may have it—is
that this approach requires foreknowledge of and a consensus
on the minimally sufficient neural underpinnings for conscious-
ness, and this is l acking. However, the bottom-up approach is still
worth exploring if a well-specified and plausible hypothesis about
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
these underpinnings can be provided. That is what we attempt to
provide with our hypothesis that sensory consciousness emerges
from the tripartite brain, isomorphic representations in neu-
ral hierarchies, and the attention-directing feature. We also re-
emphasize that our bottom-up hypothesis is not claiming fish
and amphibians have a full-blown, human-like, self-reflective
consciousness (Boly and Seth, 2012), only that they experience in-
the-moment ‘sensory mental images’ or qualia, which is all that
is required for the existence of sensory consciousness (Revonsuo,
2006).
An important basis of the human-centered, top-down
approach is that in humans and other mammals, much evidence
attributes consciousness to the large cerebral cortex and to its
interactions with the thalamus. More specifically, the many widely
distributed areas of the cortex have reciprocal (reentrant) pat-
terns of synchronized communication with one another and with
the thalamus while the RAS-related “central nuclei of the thala-
mus” subserve arousal and attention (Schiff, 2008; Edelman et al.,
2011). In humans, damage to this thalamocortical complex causes
disturbances in consciousness (Schiff et al., 2007; Boly and Seth,
2012), and there is little evidence for conscious content in any
other regions of the mammalian brain, such as the brainstem.
In birds, similarly, conscious functions are being identified in
their cerebral-cortex homologues, the Wulst and the dorsal ven-
tricular ridge (DVR) (Rose et al., 2009; Dugas-Ford et al., 2012;
Karten, 2013). Overall, this idea of the “exclusivity” of the cere-
bral cortex and thalamocor tical complex in consciousness is a
version of a “corticothalamic hypothesis” of mammalian con-
sciousness, a good summary of which is provided by Edelman
et al. (2011). A sample of the many other studies that follow or
support it includes Llinas and Ribary (2001); Baars (2002); Butler
et al. (2005); Ribary (2005); Seth et al. (2005); Butler and Cotterill
(2006); Steriade (2006); Butler (2008a); Min (2010); van Gaal and
Lamme (2012),andBaars et al. (2013).
In our view the corticothalamic hypotheses, if applied to all
vertebrates, underestimate the potential role of the optic tectum
in consciousness, specifically in fish and amphibians. That is,
these hypotheses miss the tectum’s participation in the potentially
conscious functions of recognizing and perceiving objects and
directing attention to important objects in the visual field (Dicke
and Roth, 2009; Saidel, 2009). Sophisticated visual functions are
also performed by the large tecta of birds (Shimizu et al., 2009;
Wylie et al., 2009). This raises the possibility that avian visual con-
sciousness is shared by their tectum and their visual telencephalon
(Wulst). Reptiles also have a large optic tectum, a large DVR, and
a cerebral cortex (albeit simple in nature), suggesting to us that
the tectum and dorsal pallium also share the conscious functions
in reptiles. Thus, corticothalamic hypotheses may not apply fully
to reptiles or birds.
We have proposed that the brain’s main center of sensory
consciousness shifted from the tectum to the telencephalic pal-
lium around 350–180 mya, independently in the mammalian and
sauropsid lines. Ironically, corticothalamic hypotheses of con-
sciousness (Butler et al., 2005; Edelman et al., 2005) also view
this Paleozoic/Mesozoic timeframe as pivotal, but instead assign
to it the original appearance of vertebrate consciousness in the
sauropsid/bird and mammal lines.
Another “corticothalamic” argument could be raised, against
our claim that sensory consciousness in anamniotes is tectal not
telencephalic. This argument points out that in certain fish lin-
eages the sensory telencephalon is also large and elaborate (Huesa
et al., 2009; Wullimann and Vernier, 2009a,b,c), raising the pos-
sibility of extensive pallial participation in the consciousness of
these anamniotes. In some sharks, the dorsal pallium is expanded
with higher-order sensory-processing nuclei. The same is true in
some teleosts (Prechtl et al., 1998), although within a uniquely
everted pallium that indicates an independent evolution of this
expansion in the teleost line (Wullimann and Vernier, 2009b). On
the other hand, the dorsal pallium of many other anamniotes is
small and that of lampreys is tiny, so our idea that sensory con-
sciousness in vertebrates was initially tectum-centered still holds.
However, we must admit that we may have underestimated the
potential foranincreasingroleofthedorsalpalliuminthesensory
consciousness of all the large-telencephalon vertebrates, including
those that are fish.
The corticothalamic hypotheses have difficulties of their own.
Because they are top-down, constructing and testing them means
starting with the staggering complexity of mammalian brains.
By contrast, our bottom-up approach starts with more-tractable
objects of study, namely isomorphic neural hierarchies and the
least complex of all ver tebrate brains (that of the lamprey), while
still avoiding potentially over-simplified and neurally remote
approaches to consciousness that are based on synthetic neural
modeling with computers, equations, artificial intelligence, and
robots (Reeke and Sporns, 1993; Gale et al., 2001; Franklin, 2005;
Tonini, 2008; Nageswaran et al., 2009; Ramamurthy and Franklin,
2009).
The cor ticothalamic approach, as it has been used to date,
studies only humans and other higher vertebrates in order to draw
conclusions about consciousness in lower vertebrates. This risks
lookinginexactlythewrongplacebyignoringtheonlyrelevant
study animals. It seems much better to seek anamniote unconscious-
ness and sensory consciousness directly in the fish and amphibians,
which themselves are readily available for e xperimental study.
Challenge 3: Unconscious hierarchies
The third challenge says our hypothesis is invalid if its marker
for consciousness, complex hierarchies of isomorphic representa-
tions, exists for any unconscious sensory processing. Actually, our
hypothesis does not claim that all such isomorphic hierarchies
must be conscious. We recognize that the lower levels of some
isomorphic sensory hierarchies can influence behaviors without
involving consciousness (e.g., vestibular reflexes; Kandel et al.,
2012). We also recognize that isomorphic sensory systems have
some major aspects that are conscious and others that are non-
conscious (e.g., v isual recognition of fearful or fear-expressing
faces, and the just-mentioned vestibular system; Williams et al.,
2004; Chen e t al., 2010).Anditiscertainlytruethatsome
lower-order sensory systems are not consciously perceived at all
(e.g., tendon stretch, the visceral-sensory paths from taste-like
chemoreceptors in the lining of our respiratory tubes, and barore-
ceptors in the carotid sinuses; Mescher, 2010; Kandel et al., 2012).
Additionally, many aspects of proprioception, although isomor-
phically represented, are unconscious. Merker (2005) suggests
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
such unconscious proprioception is necessary because too much
sensory information about bodily movements would confound
and contaminate the “stable reality space” of our consciousness,
thus interfering with its key role in guiding goal-directed actions.
But on the whole, we feel that consciousness uses, rather than
excludes, the important classes of sensory information. That is,
primary consciousness mainly involves the senses most vital for
survival. The intricate, consciously perceived, sensory maps of
an animal’s outer world (and inner world) lead to improved
information-gathering and better decisions on how to respond to
complex and changing environments (Plotnick et al., 2010).
Challenge 4: Unconscious perception
Numerous types of unconscious (=non-conscious) perception
have been identified in humans and could be used to argue
that lower vertebrates only have such unconscious perception
and are not conscious. Such unconscious processes, extensively
investigated, include blindsig ht, subliminal perception during
masking, binocular rivalry, attentional blink, inattentional pre-
consciousness, and implicit cognition (Baars, 2002; Kouider
and Dehaene, 2007; Ciaramelli et al., 2010; Brogaard, 2011;
Overgaard, 2012; Panagiotaropoulos et al., 2012; van Gaal and
Lamme, 2012; Baars et al., 2013). We will take these inves-
tigations at face value, ignoring the possibility that some of
their “unconscious” stimuli were actually consciously perceived
(“weakly glimpsed” or incompletely blocked: Overgaard et al.,
2008, 2013). Even so, we find several reasons why unconscious
perception in humans is mostly irrelevant to the question of
consciousness in non-mammalian anamniotes. For instance, in
humans, when compared with conscious vision, unconscious
vision is limited in duration, in flexibility, and in the strategic
use of its information for decision making (van Gaal et al., 2012),
which would compromise the survival of any animal that relied
on unconscious vision alone. Even those unconscious processes
that are most likely to influence human behavior (mismatch neg-
ativity, response inhibition, error detection, conflict resolution:
Naatanen et al., 2007; Kiefer et al., 2011; van Gaal and Lamme,
2012) are weaker than, or intimately tied to, or dependent upon,
a consc ious neural activity, which dominates the perception. It
seems that human (cerebral) unconsciousness is too intricately
linked to human (cerebral) consciousness for it to be relevant to
the non-cerebral kind of consciousness we propose for fish and
amphibians.
Perhaps the best illustration of the above considerations is
the phenomenon of blindsight. This results from damage to the
primary visual cerebral cortex, or V1, in the occipital lobe of
humans. With the affected individuals lacking primary central
visual-pathways, in the vast majority of cases their visual func-
tion is severely degraded and functionally useless, and whatever
residual, non-conscious visual functions are preserved are highly
degraded (Alexander and Cowey, 2010; Cowey, 2010; Overgaard,
2012).
Thus, a fish or frog with only blindsight or subliminal senses
would have such limited awareness as to be fast prey; it could
never survive. Even lampreys have complex behavioral adapta-
tions, dependent on vision and other senses, that far exceed
what could be produced by human paradigms of unconscious
perception. Parasitic lampreys use vision, smell, and proba-
bly electroreception to track their prey fish, to avoid danger,
locate mates, and court (Hardisty, 1979; Chung-Davidson et al.,
2004). They migrate long distances and use odors, including
pheromones, to find appropriate streams for spawning (Vrieze
and Sorensen, 2001; Vrieze et al., 2010 ). Perhaps the pinnacle of
such behavioral complexity is the sneak-mating strategy used by
male lampreys in the spawning nest, in which a sneaker male lurks
near a spawning pair, waits until the proper time, and the wraps
its body around the pair to spew its own milt onto the female’s
newly released eggs (Hume et al., 2013).Itseemstousthatsuch
intricate and varied survival functions require the heightened
awareness of sensory consciousness.
However, the fact that humans cannot perform many nor-
mal functions without consciousness does not necessarily prove
that these functions cannot be done without consciousness in
more basal vertebrates or in non-neurobiological systems. For
instance, many highly complex functions are done by computers
without consciousness (conscious inessentialism;seeMoody, 1994;
Flanagan, 1997). However, if conscious inessentialism were true
for the conscious functions of the human brain, then, theoret-
ically, the normally conscious sensory functions could also be
performed without consciousness. The problem for neurobiol-
ogy is that this leaves unexplained, for example, why certain
behavioral functions are lost in a human with a lesion in the iso-
morphic visual cortex V1, while other, non-conscious, functions
are preserved. In the human, the lost functions require conscious-
ness and the most parsimonious explanation for this seems to be
that, indeed, the documented sensory isomorphism of all primary
sensory areas of the cortex is necessary for sensory consciousness.
Nonetheless, is it still conceivable that fish, amphibians, and
reptiles exclusively use elaborate yet “unconscious” processes
in their advanced surv ival behaviors, processes that could be
unlike and far beyond the non-adaptive unconscious processes
that are typically studied in the above-mentioned human exper-
iments. The reasoned assumption of our hypothesis—that cer-
tain isomorphic neural hierarchies are required for biological
consciousness—could refute this challenge, but it does so only if
the assumption is true. Thus, our assumption must be evaluated,
by testing the predictions of our hypothesis in anamniotes, ideally
by testing them in a way similar to how the r ival, corticothalamic,
hypotheses have been tested in mammals.
TESTS TO MEET THE CHALLENGES
Our hypothesis that sensory consciousness depends on isomor-
phic hierarchies, and on the optic tectum in anamniotes, can
be tested in two ways. One way is to record the electrophys-
iological properties of the tectum, thalamus, cerebral pallium,
and reticular formation in fish and amphibians, expanding on
the thalamocortical recordings reviewed by Llinas and Steriade
(2006), but focusing on the thalamo-tectal interactions in these
anamniotes. Reentrant and recurrent processing should be sought
between thalamus and tectum, as should oscillatory synchronicity
of the firing neurons. Recurrent processing (van Gaal and Lamme,
2012) means that whenever sensory information reaches a succes-
sive level in a hierarchy, the hig her level sends signals back to the
lower levels, as has especially been demonstrated in the cerebrum
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
of higher primates. This recurrent interaction could be a hallmark
of consciousness because it combines information from many
different brain regions and its reverberations allow it to retain
information over time. Forward-then-recurrent signals should be
easy to detect with the recording electrodes. Large, sluggish frogs
and young zebrafish (Ahrens et al., 2012) should be the best test
animals for the brain recordings we propose.
Another test is to perform such recordings on reptile brains.
Reptiles are the key transitional group for all the hypotheses of
consciousness considered in this paper, yet the y are exceptionally
poorly studied with regard to sensory processing and sensory con-
sciousness ( Butler and Cotterill, 2006; Jarvis, 2009; Dugas-Ford
et al., 2012).
DIFFERENT GENES AND DIFFERENT EVOLUTIONARY TRAJECTORIES
Can the genes we have related to consciousness tell anything about
the origin and earliest evolution of the conscious process? One
might predict that the developmental pathways involved in the
different aspects of isomorphism share genes and gene circuits in
common, at least in the fundamental, early expressed stages of
these pathways, and that these shared genes should derive from
the visual pathway if vision was the ancestral sense around which
all other senses were patterned (Butler, 2000; Shepherd, 2012).
But this prediction fails for se veral reasons. The gene-expression
pathways in the different kinds of ectodermal placodes differ
from one another (Graham and Shimeld, 2012)—although these
differences can be explained as separate ways to direct the pla-
codesawayfromthedefault,ancestralstateofdevelopinginto
the lens placode of the visual system (Bailey et al., 2006). This
lens-as-template finding rescues the “vision-first” hypothesis, but
then, comparisons of the all-important placodes with the neural
crest proceed to reveal even more genetic disunity. For example
the neural-crest specifiers (transcription factors Snail1/2, FoxD3,
Twist) differ markedly from the placode specifiers (Six1, Six4,
Eya) (Yu, 2010; Graham and Shimeld, 2012). In fact, Schlosser
(2008) demonstrated in depth that the neural crest and placodes
differ from each other not only in their specifier genes, but also
in the upstream gene pathways that induce their formation in
the first place, which led him to conclude the crest and placodes
evolved independently of one another from the dorsal ectoderm
(also supported by Sestak et al., 2013). And the “isomorphism”
genes we listed in the “Genes and Consciousness” section as estab-
lishing trigeminal-somatotopy (Hoxa2), vs. retinotopy (EphrinA,
En-1, En-2), vs. tonotopy (Tnc, Nov, Slo) all differ from each
other. Thus, the modules of the isomorphic neural hierarchy show
no genetic commonality, judging from the available data. This
implies that when the definitive placodes and neural crest e volved
as key adaptations in pre-vertebrates in the Early Cambrian, the
genetic signals for patterning the different senses diverged rapidly
into a multitude of different directions and pathways. It also
implies that many aspects of isomorphic mapping in the nervous
system evolved independently among the different senses.
Similarly, consciousness itself (as we have proposed it) appears
to have advanced throug h somewhat different paths in differ-
ent lines of vertebrates. One example is the tectal conscious-
ness of anamniotes vs. the pallial consciousness of amniotes.
Another, puzzling, example comes from comparing the pallial
consciousness of birds vs. mammals. While birds are capable of
many advanced cognitive abilities such as demonst rating working
memor y and episodic memory, learning, category formation, tool
use, number concepts, and object permanence (Butler et al., 2005;
Edelman et al., 2005; Butler, 2008a; Edelman and Seth, 2009), the
pallial regions involved seem to differ from those of mammals
that have these same abilities. That is, the bird’s Wulst and DVR
do not obviously resemble the mammal’s cerebral cortex in gross
anatomy nor in the microscopic anatomy that could be studied
by traditional microscopic methods. This led to much contro-
versy over the avian homologue of the mammalian cerebral cor tex
(Reiner, 2005; Medina, 2009; Butler et al., 2011).
New studies finally solved this puzzle (Wang et al., 2010;
Kaas, 2011; Dugas-Ford et al., 2012; Karten, 2013), by confirm-
ing that the laminated cerebral cortex of mammals corresponds to
both the non-laminated DVR and the pseudo-laminated Wulst of
birds, as well as to the DVR and simpler cerebral cortex of reptiles.
The studies succeeded by showing that in the three animal groups
these brain regions have comparable gene-expression patterns (by
EAG2, RORB, ER81, PCP4), as well as comparable afferent and
efferent connections (also see Jarvis, 2009; Kalman, 2009;and
Butler et al., 2011). In addition, the new studies revealed a nearly
identical internal microcircuitry in birds and mammals. Finally
and most importantly, the corresponding avian and mammalian
regions are known to feature the same kinds of retinotopic,
somatotopic, and tonotopic maps, as well as similar higher-order
sensory processing centers (Adamo and King, 1967; Karten, 1968,
1969; Karten et al., 1973; Pettigrew and Konishi, 1976; Pettigrew,
1979; Wild, 1987; Wang et al., 2010). Thus, despite some diver-
gent and parallel evolution of their homologous pallial regions,
the large-brained mammals and birds should share ways of gener-
ating higher sensory consciousness with hierarchical organization
and isomorphic maps.
CONCLUSION
This is the first hypothesis that dates the origin of consciousness,
explains its neural architecture, explores its genetics, identifies the
most basal animal that has it, and accommodates its neurobiol-
ogy with the “hard problem” of consciousness and subjectivity,
all knitted together in one model. We hypothesize that primary
or sensory consciousness stems from a confluence of neurologi-
cal features common to all vertebrates (Table 2 ), especially from
multiple, reciprocally connected, isomorphic representations at
different hierarchical levels within the nervous system. These fea-
tures co-emerged, probably in a rather short interval of time,
between 560 and 520 mya (Ta b l e 3). Perhaps over half a billion
years old, consciousness may be hundreds of millions of years
older than investigators have supposed, so we cannot assign it
exclusively to the animals with the highest intellectual capacities,
such as humans, apes, and porpoises. We also hypothesize that
from the start, sensory consciousness and the existence of qualia
acted as a prime mover of vertebrate evolution by allowing verte-
brates to go beyond mere reflexes and to map, then assess, their
external and internal environments in exquisite detail.
We offer a “two step hypothesis” in which the neural center of
primary consciousness first evolved in Cambrian anamniotes as
multimodal and isomorphic sensory representations dependent
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Feinberg and Mallatt The evolutionary and genetic origins of consciousness in the Cambrian
on the visual tectum and its interconnections with the thalamus
and reticular formation. Second, in reptiles of the pre-mammal
and sauropsid lineages, the enlarging dorsal pallium gradually
became the dominant center of sensory consciousness, mostly
independently in the two l ineages. The timing for this second
step at 350–180 mya corresponds to the initial emergence of con-
sciousness in rival, corticothalamic hypotheses (Butler et al., 2005;
Edelman et al., 2005).
We urge that more research be performed directly on con-
scious and unconscious senses in anamniotes and reptiles, rather
than inferring the mental states of such vertebrates based on the
mammalian (and avian) pallium and thalamus, which may be
poor models.
We further posit that there is a common genetic basis for con-
sciousness, not shared among all the different senses, but shared
within the individual sensory systems across the vertebrate groups
(fish, amphibians, reptiles, birds, and mammals). Some of the
important genes are now known (Tab l e 2 ), and many more will
undoubtedly be discovered. These genes may be useful mark-
ers for the presence of primary consciousness. Assuming that
consciousness in invertebrates either does not exist or that it arose
later (e.g., in cephalopods, see Kroger et al., 2011), then the most
basal conscious organisms on earth are the jawless vertebrates,
represented by the lamprey.
Finally, given the existence of isomorphic neurohierarchical
processing in all vertebrates, the neuroontologically unique and
irreducible features of sensory consciousness appear to require
successive re-representations of mapped sensory information
throughout the levels, coupled with a global activation system
(Feinberg, 2009, 2011, 2012). The qualitative “feel” of these sen-
sor y images had its origin in sensory receptors that subsequently
proceeded to evolve and specialize within the hier archical path-
ways. In evolution, these systems began as simple, unconscious
reflexes (e.g., the light spot-initiating reflexes in amphioxus, or
nociceptors stimulating reflexive withdrawal), but as the central
structures evolved to process this activity, hierarchically arranged
neural-neural interactions created conscious sensory images and
their associated qualia (Feinberg, 2012). This made sensory
consciousness into the unique neurobiological system feature that
it is.
ACKNOWLEDGMENTS
We wish to express our thanks to the many investigators who
kindly gave advice and shared their wisdom in the course of
the writing of this paper. Our appreciation especially goes to
Ann Butler who patiently answered many questions on verte-
brate neuroanatomy and evolution. Also our thanks for help-
ful input from Gerhard Schlosser, Trevor Lamb, Bjorn Merker,
Harvey Karten, Georg Striedter, Laura Bruce, Jon Kaas, Gordon
Shepherd, Andrew Parker, Mario Wullimann, Giandomenico
Iannetti, Frances Lefcort, Lynn George, Barry Stein, Maria
Fitzgerald, Jun-Yuan Chen, Brian Hall, Bud Craig, Berit Brogaard,
and Anil Seth. While this project has greatly benefited from their
invaluable assistance, none of course are responsible for the con-
tent or opinions expressed in this paper. Finally, we thank Jill
Gregory for fine work on the illustrations.
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Conflict of Interest Statement: The
authors declare that the research
was conducted in the absence of any
commercial or financial relationships
that could be construed as a potential
conflict of interest.
Received: 28 March 2013; accepted: 05
September 2013; published online: 04
October 2013.
Citation: Feinberg TE and Mallatt J
(2013) The evolutionary and genetic ori-
gins of consciousness in the Cambrian
Period over 500 million years ago.
Front. Psychol. 4:667. doi: 10.3389/fpsyg.
2013.00667
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