Evolution of consciousness: Phylogeny, ontogeny,
and emergence from general anesthesia
George A. Mashour
and Michael T. Alkire
Departments of Anesthesiology and Neurosurgery, Neuroscience Graduate Program, University of Michigan Medical School, Ann Arbor, MI 48109; and
Veterans Administration Long Beach Healthcare System, Department of Anesthesiology and Perioperative Care, Center for the Neurobiology of Learning
and Memory, University of California, Irvine, CA 92697
Edited by Francisco J. Ayala, University of California, Irvine, CA, and approved April 9, 2013 (received for review February 11, 2013)
Are animals conscious? If so, when did consciousness evolve? We
address these long-standing and essential questions using a modern
neuroscientiﬁc approach that draws on diverse ﬁelds such as con-
sciousness studies, evolutionary neurobiology, animal psychology,
and anesthesiology. We propose that the stepwise emergence from
general anesthesia can serve as a reproducible model to study the
evolution of consciousness across various species and use current data
from anesthesiology to shed light on the phylogeny of consciousness.
Ultimately, we conclude that the neurobiological structure of the
vertebrate central nervous system is evolutionarily ancient and highly
conserved across species and that the basic neurophysiologic mecha-
nisms supporting consciousness in humans are found at the earliest
points of vertebrate brain evolution. Thus, in agreement with Darwin’s
insight and the recent “Cambridge Declaration on Consciousness in
Non-Human Animals,”a review of modern scientiﬁc data suggests
that the differences between species in terms of the ability to experi-
ence the world is one of degree and not kind.
Evolutionary biology forms a cornerstone of the life sciences and
thus the neurosciences, yet the emergence of consciousness
during the timeline of evolution remains opaque. As the theory of
evolution began to eclipse both religious explanations and Enlight-
enment doctrines regarding the singularity of human consciousness,
it became clear that consciousness must have a point of emergence
duringevolution andthat point likelyoccurred before Homo sapiens.
“How,”Darwin questioned, “does consciousness commence?”His
post-Beagle research on this question evidently caused him violent
headaches. One such headache can be expressed as the 20th century
philosophical distinction of phenomenal consciousness and access
consciousness (1). Phenomenal consciousness relates solely to sub-
jective experience, whereas access consciousness includes (among
other processes) the ability to report such experiences verbally
(otherdistinctions related to consciousness can befound in Table 1).
Thus, thescientist looking for objectiveindices of subjective events is
primarily limited to humans manifesting access consciousness, an
obstacle in studying the evolution of consciousness antecedent to
our species. We could, however, take solace in the dictum that on-
togeny recapitulates phylogeny and search for clues in developing
humans. Unfortunately, Haeckel’s theory of recapitulation is not
scientiﬁcally sound and, even if applicable in this case, we would still
be constrained by the high probability that babies develop phe-
nomenal consciousness before access consciousness. To overcome
the limitations in identifying the birth of consciousness, we need
a reproducible experimental model in which (i) consciousness
emerges from unconsciousness at a discrete and measurable point,
(ii) phenomenal consciousness and access consciousness are closely
juxtaposed or collapsed, and (iii) assessment of neural structure and
function is possible. In this article, we consider top-down and bot-
tom-up approaches to consciousness, nonhumanconsciousness, and
the emergence of consciousness from general anesthesia as a model
for the evolution of subjectivity.
Top-Down and Bottom-Up Approaches to Consciousness
To locate the birth of consciousness on the evolutionary time-
line, it will be beneﬁcial to consider the basic neural machinery
that is thought to be involved in human consciousness (2–8). The
distinction between phenomenal and access consciousness was
noted, but phenomenal consciousness itself reﬂects the disso-
ciable neurobiological processes of awareness and arousal (9–13)
(Table 1). Awareness refers to the content of consciousness (red
apple vs. blue sky), whereas arousal refers to brain activation and
level-of-consciousness (alert vs. drowsy vs. asleep vs. anesthetized).
A number of current theories about consciousness propose that
the cortex is the primary site containing the neural correlates of
awareness (14–19), whereas midline subcortical brain structures
provide ascending arousal inﬂuences to the cortex (15, 17, 19).
Thus, we can explore both top-down and bottom-up approaches
Top-Down Approach. Seth et al. (14) propose three main physio-
logical reasons supporting the importance of the neocortex to
the process of consciousness. First, the electroencephalogram
of virtually all mammals and birds in the awake state is charac-
terized by desynchronized, high-frequency, and low-amplitude
activity. This pattern changes to one of low-frequency, high-
amplitude activity during depressed levels of consciousness such
as nonrapid eye movement (NREM) sleep, minimally conscious
states, and anesthesia. Thus, a state-dependent change in the
electrical ﬁring properties of the neurons across the neocortex
varies with the level of arousal and strongly supports the idea
that neuronal activity in the brain (and particularly in the neo-
cortex) is a necessary requirement for consciousness (20).
Second, consciousness appears to be linked more speciﬁcally
with neural activity in the thalamocortical system. In this view,
the midline brain structures of brainstem and midbrain are thought
to be important for keeping the cortex in an aroused or awake
state, whereas the cortical regions are thought to serve as speciﬁc
cognitive modules contributing to the contents of conscious ex-
perience. The idea that certain brain regions are more important
than others for generating the contents of consciousness is fur-
ther supported by a number of basic neurological facts. For in-
stance, a person could suffer the loss of the cerebellum or large
bilateral portions of the medial temporal lobes, including
amygdala and hippocampus complex, and would not become
unconscious. However, focal damage to speciﬁc areas of cortical
tissue will change the contents of a person’s consciousness in
a way that matches the loss of function associated with the
speciﬁc area damaged. Cortical lesions can thus result in such
speciﬁc impairments of consciousness that one may no longer be
able to speak, perceive color, or identify parts of themselves as
their own (21). Damage to lower midline brain structures, on the
This paper results from the Arthur M. Sackler Colloquium of the National Academy of
Sciences, “In the Light of Evolution VII: The Human Mental Machinery,”held January
10–12, 2013, at the Arnold and Mabel Beckman Center of the National Academies of
Sciences and Engineering in Irvine, CA. The complete program and audio ﬁles of most
presentations are available on the NAS Web site at www.nasonline.org/evolution_vii.
Author contributions: G.A.M. and M.T.A. wrote the paper.
The authors declare no conﬂict of interest.
This article is a PNAS Direct Submission.
To whom correspondence should be addressed. E-mail: email@example.com.
June 18, 2013
other hand, will likely alter the level of consciousness (i.e., arousal)
without necessarily changing its contents.
Thalamocortical oscillations have been posited to be of critical
importance to consciousness because they help integrate func-
tionally diverse and spatially distinct cognitive modules in the
cortex (22, 23). The interplay of segregation and integration is
a fundamental focus of the integrated information theory of con-
sciousness (8, 24). The capacity of the thalamocortical system to
achieve both integration and differentiation is reﬂected in higher
levels of Phi, a proposed metric for consciousness (8). Phi reﬂects
the amount of information generated by an integrated system
beyond the information contained within the components of the
system. In principle, this measure captures the emergent property
of the system (consciousness) that cannot be causally reduced to
individual subsystems (particular brain regions). Phi is predicted to
decrease during sleep and seizures; preliminary evidence suggests
it also decreases during anesthesia (25), possibly due to impaired
long-range coupling of neural spike activity (26). Although the
integrated information theory of consciousness has yet to be de-
ﬁnitively demonstrated, it is a guiding paradigm that can inform
the evolution of consciousness from the network perspective.
Creatures with brain network systems that are capable of gener-
ating high values of Phi are more likely to be conscious (27).
Third, widespread brain activity appears correlated with con-
scious activity. Sensory input spreads quickly from sensory cortex
to parietal, temporal, and prefrontal areas (28). This spread of
cortical activity is also associated with recurrent local feedback
occurring along the way, followed shortly thereafter by long-
range feedback from anterior to posterior structures (29). These
long-range connections are thought to be important for the ex-
periential aspects of consciousness (i.e., awareness) (30) and
appear to be preferentially suppressed during general anesthesia
(26, 31). In particular, there is strong evidence that networks
across the frontal and parietal cortices are associated with
awareness across multiple sensory modalities (32–34). The lat-
eral frontoparietal network plays a role in mediating conscious-
ness of the environment, whereas the medial frontoparietal
network plays a role in mediating internal conscious states such
as dreaming and internally directed attention (35, 36). It is be-
coming increasingly clear that the directionality of corticocortical
network communication is relevant to conscious processing. In-
formation processing from the caudal to rostral direction (feed-
forward) is associated with sensory processing that can occur in
the absence of consciousness (e.g., general anesthesia, priming)
(37, 38). In contrast, information processing in the rostral-to-
caudal direction (feedback or cortical reafference) is thought to
be associated with experience itself and is preferentially inhibited
by general anesthetics (38–40).
The neocortical view of consciousness originates, in part, from
early morphologic examination of brain differences across species
that suggested the capacities of consciousness increased as brains
evolved from more primitive reptilian organization, to mammalian
(or, with a limbic system, paleomammalian), and then neo-
mammalian organization, characterized by an intricately folded
neocortex. This conceptualization of brain evolution occurring in
stages during which more “advanced”brains—along with their ex-
panded behavioral repertoire—were built on the structure of earlier
forms was popularized by Maclean as “the triune brain”(41). Im-
portantly, this view of brain evolution is now largely considered er-
roneous (42, 43). It did offer an easy conceptualization for relating
brain structure with function and suggested evolutionary time points
for when various behaviors would have emerged. Newer ﬁndings,
however, strongly refute the model of a triune brain, especially the
concept of a later developing neocortex (Fig. 1) (42). As it turns out,
a precursor of the neocortex was actually present in the earliest
evolving vertebrates, a claim based on some aspects of connectivity
and homology of early transcription factor expression (44). The basic
structural pattern of a brainstem, midbrain, and forebrain did not
need to be completely reinvented as each new species emerged.
Rather, as various ecological niches were exploited by various crea-
tures, those brain regions best suited for enhancing survival in the
local environment were emphasized for further development (42).
Bottom-Up Approach. Since the discovery of the ascending re-
ticular activating system by Moruzzi and Magoun in the late
1940s (45), the fundamental and permissive role for arousal in
generating conscious states has been well established. It is now
Table 1. Deﬁnitions relevant to consciousness
Easy vs. hard problem of consciousness This distinction was drawn by philosopher David Chalmers. “Easy”
problems of consciousness (which are easy in principle only) include
understanding the neural basis of feature detection, integration,
verbal report, etc. The hard problem is the problem of experience;
even if we understand everything about neural function, it is not
clear how that would explain subjectivity.
Awareness Cognitive neuroscientists and philosophers use the term “awareness”
to mean only subjective experience. In clinical anesthesiology, the
term awareness is (inaccurately) used to include both consciousness
and explicit episodic memory.
Wakefulness vs. awareness Wakefulness refers to brain arousal, which can be manifest by
sleep–wake cycles and can occur even in pathologic conditions of
unconsciousness such as vegetative states. Thus, being awake is
dissociable from being aware.
Phenomenal vs. access consciousness Phenomenal consciousness is subjective experience itself, whereas access
consciousness is that which is available to other cognitive processes
(such as working memory or verbal report).
External vs. Internal consciousness External consciousness is the experience of environmental stimuli
(such as the sound of an orchestra), whereas internal consciousness is
an endogenous experience (such as a dream state).
Consciousness vs. responsiveness An individual may fully experience a stimulus (such as the command
“Open your eyes!”) but not be able to respond (as when a patient is
paralyzed but conscious during surgery).
Levels of consciousness vs. contents of consciousness Levels of consciousness include distinctions such as alert vs. drowsy vs.
anesthetized, whereas the contents of consciousness refer to particular
phenomenal aspects such as a red rose vs. a blue ball.
www.pnas.org/cgi/doi/10.1073/pnas.1301188110 Mashour and Alkire
clear how a number of speciﬁc nuclei and speciﬁc cell types within
the brainstem, midbrain, basal forebrain, and diencephalon send
long-range axons throughout the cortex to enhance arousal and
generate a neurochemical environment in the cortex that is ca-
pable of supporting consciousness (11). The role of arousal in
regulating overall levels of consciousness is clearly established in
connection with depressed levels of consciousness as during sleep
or coma (46). How arousal machinery interacts with conscious-
ness during more subtle cognitive and behavioral manipulations is
the subject of much current research (47–49). However, through
the study of arousal as it relates to emotion (50, 51), another link
is made that puts some of Darwin’s later investigations into
a more modern light.
Darwin spent the later years of his career investigating the
similarities and differences associated with emotional expression
in man and animals (52). He reasoned that if animals show
emotion through behavioral expression, and man is an animal,
then the behavioral expression of emotion in man must share
a similar neurobiologic evolution with the other animals capable
of expressing similar emotions. Put another way, years before
behaviorism dominated neuroscience, Darwin saw how com-
monalities in emotional expression across species likely reﬂected
the occurrence of similar underlying states of mind that only
made sense within a theory of evolution. Modern study into the
emotional lives of animals now reveals how fundamentally sim-
ilar the brain structures are that support affective reactions in
animals and humans (53).
Consciousness may not have emerged from the need to make
an internal representation of the outside world, but rather as an
extension of very basic primitive or primordial emotional inﬂu-
ences. Such emotional inﬂuences would generate an arousal
response in an organism and prepare its brain for action. This
hypothesis is well elaborated by Denton in his book on primor-
dial emotions (6). It posits that the most basic instincts, such
as thirst, hunger for air, hunger for salt and food, and the
desire for sex are the deﬁning starting points for evolving
a conscious brain (36). This idea holds within it the concept of
intention, desire, and action selection, where the basic intention
of a movement is in the service of fulﬁlling a desire. As noted by
Darwin (52), “So strongly are our intentions and movements
associated together, that if we eagerly wish an object to move in
any direction, we can hardly avoid moving our bodies in the same
direction, although we may be perfectly aware that this can have
The basic behavior of an organism is driven by a fundamental
physiologic need to maintain homeostasis. Those cells and
systems used for monitoring and maintaining the internal milieu
are referred to as interoceptors (6). The basic behaviors driving
homeostasis are evident as far back as the ﬁrst multicellular
organisms that needed a vascular system to provide nutrients
to those cells no longer exposed directly to the environment.
Creatures that could meet their basic homeostatic needs are the
ones that survived; those that did not suffered extinction. The
brain structures needed for generating arousal and primitive
emotional responses are generally located in the brainstem,
midbrain, and limbic system and are as old as the vertebrate
radiation itself (54).
Recent work on the lamprey, a jawless ﬁsh whose common
ancestor forms the basis for all vertebrates more than 500 million
years ago, has revealed just how ancient the neuroanatomy and
neurochemistry needed for action selection is. Findings reveal
that the lamprey’s behavioral motor output system shows similar
complexity to higher-level vertebrates who are capable of regu-
lating behavior by both direct and indirect motor output pathways
from the basal ganglia (55). In other words, the lamprey is capable
of both selecting a motor output to perform and at the same time
inhibiting the performance of other possible outputs. Thus, they
are capable of making a choice depending on the situation with
which they are confronted. This “reduction of uncertainty”(a
classic deﬁnition of information) through action selection may be
the precursor to the highly informative states of consciousness
characteristic of humans. We address the relationship of motoric
behavior and consciousness in the next section.
More complex neocortical abilities offered a survival advan-
tage to more complex brains by giving organisms a larger grasp of
their surroundings, but these systems developed over time and
used sensory information from the environment or exteroreceptors
(6). Denton illustrates his point with the example of a dehydrated
frog placed next to a water source in the sun. The frog has only
a limited capacity in its visual system and when placed next to
a source of water it will usually die without moving, unless it
stumbles on the water by accident. If, by chance, the frog ﬁnds the
water, it will drink, which suggests functioning interoreceptors. In
contrast, the more highly evolved visual system of the lizard allows
that creature to see the water and immediately drink, suggesting
that its more evolved brain more successfully couples its extero-
receptor-mediated perceptions with its interoreceptor-mediated
needs. This coupling of an internally based need system with an
externally based situational awareness system is likely the foun-
dation for the emergence of consciousness, and it closely corre-
sponds to the mental machinery seen in humans for generating
awareness and arousal.
The brainstem arousal centers are, for the most part, juxta-
posed with the sensory motor inputs and outputs of the cranial
nerves that supply the head and neck with its ability to orient
a creature to its environment and provide a stable platform for
sensing its surroundings. The motor output of the cranial nerves
is fundamentally linked with the expression of emotion in es-
sentially all vertebrates, and this likely emanates from the oldest
of the predator–prey relationships. In essence, an open mouth
signiﬁes a meal for the predator, and if the hunt is successful, it
would likely be associated with internal sensations of goal/task
completion that would serve to fulﬁll a basic need for food in the
predator. This goal completion/desire fulﬁllment would likely
have positive reinforcing value for an organism and might easily
be hypothesized to lead to internal states comparable to a sense
of pleasure (53). For the prey, an open mouth heading toward it
would certainly be cause for alarm, prompting an immediate
escape response that, if successful, might be associated with an
internal state of heightened arousal and fear (53). Thus, the most
basic emotions and arousal states are associated with internal
feedback networks that serve to guide an organism’s behavior
toward its best possible situational outcome. This emotional
arousal machinery underlies essentially all behavioral choices in
the vertebrate brain.
Fig. 1. Theories of brain evolution. Ancient brain structure evolution theory
of Scala Naturae showing brain development proceeding from simple to
more complicated with the addition of new brain regions as evolution
progressed. This erroneous view is compared with a modern understanding
of brain structure evolution that reveals a basic common structure evolved in
the vertebrate brain and various regions expanded to accommodate each
speciﬁc animal’s needs. Modiﬁed from (42) with permission from Elsevier.
Mashour and Alkire PNAS
June 18, 2013
Consciousness in Nonhuman Species
If consciousness evolved in conjunction with cephalad develop-
ment of the central nervous system, then its emergence should, in
principle, be identiﬁable at a discrete point on thetree of evolution.
Darwin reasoned that the cognitive differences between species
must be one of degree and not kind. This conclusion is consistent
with the recent Cambridge declaration that occurred on July 7,
2012, at the ﬁrst annual Francis Crick memorial conference on
consciousness.A group of prominent scientists formally declared in
a document entitled the “Cambridge Declaration on Conscious-
ness in Non-Human Animals”that the neurobiological structures
needed to support consciousness are not uniquely human (56). This
declaration essentially states that the capacity for consciousness
likely emerged very early in evolutionaryterms, and those processes
that support consciousness in humans are likely characteristic of
many living creatures. In fact, according to the declaration, based
on a number of considerations from comparative brain anatomy
and current knowledge about the neurobiology of consciousness, it
would seem almost certain that some form of consciousness is
present in all mammals and could have emerged on the evolu-
tionary timeline at the branch point of amniotes.
However, long before the Cambridge declaration, some thinkers
expressed serious concerns about attributing higher levels of con-
sciousness to all life. Indeed, Rene Descartes, often considered the
philosophical father of the mind–body relationship, questioned
whether a conscious self arose in the animal kingdom. He avoided
ascribing a conscious self to a particular animal because by doing so
he recognized that he mightbe compelled to ascribe a conscious self
to all animals. This all or none approach did not reﬂect an evolu-
tionary theory perspective, which raised the possibility of a con-
scious continuum. This continuum, however, also introduces
difﬁculty. As pointed out by Gallup, in discussing the emergence of
consciousness in animals (57), “Where do we draw the line? On the
one hand, we could decide not to draw a line. This would presume
that all living things are sentient, conscious, and mindful. While the
data are admittedly incomplete, the issue should be taken seri-
ously. Life on this planet consists of several million different spe-
cies. Most are microorganisms, plants, and insects. I doubt that
there is a paramecium, a rosebush, or a termite alive today which is
aware of its own existence or has the capacity to become the object
of its own attention.”With Gallup’s statement, we begin to see the
need for clarity in how or why we associate certain behaviors with
subjective experience and the need for some operational deﬁ-
nitions of the “consciousness”being studied.
To identify the origin of sentience along an evolutionary time-
line, it is beneﬁcial to consider a common element that might link
consciousness across species, rather than focusing on the ostensibly
unique qualities of human experience such as self-reﬂection.
Furthermore, this common element should likely relate to a goal-
directed behavior or response pattern that confers a survival
advantage in a given environment. In line with philosophers such
as Merleau-Ponty and neuroscientists such as Rudolfo Llinás and
György Buzsáki, we support motility (also referred to in this
context as motricity) as a strong candidate for the evolutionary
anlage of consciousness (58, 59). Consider, for example, the
unicellular paramecium, which is covered with several thousand
cilia. These cilia can serve both the function of sensing envi-
ronmental stimuli and initiating motility responses (e.g., attrac-
tion, avoidance) based on the nature of those stimuli. This
preneural example of a single structure (i.e., cilia and their co-
ordinated activity) mediating both sensation and response is in-
triguing but does not establish the primacy of motility as a kernel
of consciousness. Perhaps a more compelling case is that of the
sessile sea squirt, which possesses neural structures only tran-
siently during a larval stage (60). Neural ganglia and primordial
sensory processing allow the sea squirt to ﬁnd a suitable local
environment and underwater surface for attachment. However,
after this goal is achieved the neural tissue is digested, suggesting
a role related exclusively to movement. Although it is unlikely
that paramecia and sea squirts have phenomenal experience,
these early examples of sensation in the service of motility lead
us to start the search for the neurobiological origins of con-
sciousness in phylogenetically conserved structures.
What Is the Neural “Core”of Consciousness?
To identify which aspects of the mental machinery should be the
focus of evolutionary consideration for consciousness, we need
to identify the neural correlates of the most primitive core of
human consciousness. The still emerging ﬁeld of consciousness
studies has been dominated in the last decade by a search for the
neural correlates of consciousness, which have been deﬁned as
the speciﬁc and minimally adequate brain states that correspond
to states of consciousness (61). However, studies of the content
of consciousness (e.g., the awareness of a red rose placed in your
visual ﬁeld) already assume a conscious brain; thus, the neural
activity or structure identiﬁed in these paradigms correspond to a
speciﬁc content within a preexisting consciousness (62). Studying
the level of consciousness (e.g., arousal states) is also beset with
difﬁculties. For example, the transition from a fully conscious to
unconscious state will inform us primarily of correlates required
for the full spectrum of waking human consciousness rather than
the minimal or core requirements. Furthermore, we must also
grapple with how to identify the true correlate (or substrate) of
consciousness vs. neural prerequisites or neural consequences of
consciousness (63, 64).
To address some of these difﬁculties, a recent study explored
the neural correlates of the primitive form of consciousness that
arises during emergence from general anesthesia (65). With
anesthesia, the level of consciousness can be manipulated as an
experimental variable, and the resultant changes in brain activity
can then be determined with various neuroimaging and neuro-
physiologic techniques. Numerous studies have now examined
what happens to brain activity when consciousness is removed by
anesthesia (66, 67); however, fewer studies have investigated the
correlates of consciousness associated with its return following
a period of anesthesia (68–71). In one recent study of healthy
male volunteers, positron emission tomography (PET) was used
to investigate the neural correlates of the recovery of con-
sciousness from the i.v. anesthetics propofol and dexmedeto-
midine (65). The order of the state transition is important
because the investigation of consciousness to unconsciousness
may yield a variety of nonspeciﬁc deactivations due to drug
effects that do not necessarily play a core role in consciousness.
The emergence of consciousness (as judged by the return of
a response to command) was correlated primarily with activity of
the brainstem (locus coeruleus), hypothalamus, thalamus, and
anterior cingulate (medial prefrontal area). Surprisingly, there
was limited neocortical involvement that correlated with this
primitive form of consciousness. Frontal–parietal connectivity
appeared to be the key cortical response, which has been con-
ﬁrmed by studies of consciousness and anesthesia using electro-
encephalography (70). Similar ﬁndings were seen in another
imaging study investigating the emergence of consciousness from
sleep (72). In the sleep study, midline arousal structures of the
thalamus and brainstem also recovered function well before
cortical connectivity resumed. Thus, the core of human con-
sciousness appears to be associated primarily with phylogeneti-
cally ancient structures mediating arousal and activated by
primitive emotions (36, 73), in conjunction with limited connec-
tivity patterns in frontal–parietal networks (74, 75) (Fig. 2).
The emergence from general anesthesia may be of particular
interest to evolutionary biology, as it is observed clinically to prog-
ress from primitive homeostatic functions (such as breathing) to
evidence of arousal (such as responsiveness to pain or eye opening)
to consciousness of the environment (as evidenced by the ability to
follow a command) to higher cognitive function. Unlike the emer-
gence of consciousness over millions of years in phylogeny or
months during the gestational period in ontogeny, the emergence
www.pnas.org/cgi/doi/10.1073/pnas.1301188110 Mashour and Alkire
of consciousness from the anesthetized state is a reproducible
model system that can be observed in real time over the course of
hours. Multimodal investigation using neuroimaging and neuro-
physiology, in conjunction with clinical observation and cognitive
evaluation, could uncover key shifts of neural activation or network
organization that support conscious processing. For example, high-
density electroencephalography could be used during recovery
from general anesthesia to measure Phi to help delineate in
humans the threshold for emerging consciousness. Such a thresh-
old could then be compared with other species in the waking state
to determine the relative value with reference to the neural core of
human consciousness. This approach could be applied to any
number of brain network properties, as assessed quantitatively
through graph theoretical methods (76).
Network approaches—which have broad applicability in mathe-
matics, biology, computer science, and sociology—might be par-
ticularly attractive to test hypotheses across species, where func-
tionally similar cognitive systems may arise from neurobiologically
distinct structures. For example, the mammalian cortex and avian
pallium are histologically distinct (Table 2) (77), but may subserve
similar network functions that can be quantitatively assessed and
compared with human ﬁndings. General anesthesia represents
a way of turning back the evolutionary clock of cognitive function
in humans and—depending on the “depth”and length of anes-
thetic exposure—allows investigators to observe the return of
neural function in a way that could recapitulate phylogeny.
Although not without difﬁculties (including the contamination of
access consciousness, because language is involved in assessing
return of consciousness after anesthesia), advantages of emer-
gence from anesthesia as a model system for the evolution of
consciousness include convenience, reproducibility, real-time
observation, possibility of subjective report of experiences (with
experiments in humans), and amenability to neuroscientiﬁc in-
vestigation across multiple species.
When Does Consciousness of the World Arise?
The recent experiments with general anesthesia in humans sug-
gest that phylogenetically ancient structures in the brainstem and
diencephalon—with only limited neocortical involvement—are
sufﬁcient to support primitive consciousness. Where, then, does
consciousness arise on the evolutionary timeline? One might be
tempted to conclude that consciousness commenced as our
mammalian ancestors evolved just beyond reptiles and their pre-
dominantly subcortical brains. However, paleontological ﬁndings
suggest that the synapsid line that gave rise to mammals and the
sauropsid line that gave rise to reptiles and birds both diverged
from the primitive anapsid line at a single point ∼315 million years
ago (78). Furthermore, there is signiﬁcant evidence that avian
species are capable of higher cognition and even consciousness
itself (79). For example, birds demonstrate evidence of explicit
episodic recall (i.e., conscious memory of an event) (80) and
theory of mind (i.e., attribution of subjective mental events to
another being) (81). Thus, it would be misguided to try to identify
a single point at which consciousness emerged because evidence
suggests that consciousness evolved along two independent line-
ages. As pointed out by Butler et al. (82), birds and mammals
share a number of homologous traits despite this evolutionary
divergence, including a dramatic increase in their brain–body ra-
tios (compared with reptiles), homeothermy, extended parental
care of offspring, habitual bipedalism, distinct sleep stages, and
complex social interactions. The neurobiology also reﬂects ho-
mologous advances, particularly in the mammalian neocortex and
the avian pallium (Table 2). These advances include the emer-
gence of recurrent or feedback processing, which is not found in
reptiles. Thus, both birds and early mammals are equipped with
a neural substrate consistent with conscious processing: phyloge-
netically conserved brainstem, diencephalic structures such as
thalamus and hypothalamus, and association neocortex (or
equivalent) capable of recurrent processing. All of these struc-
tures appear to play a role as the neural core for primitive con-
sciousness in humans, as evidenced by experiments with
The critical role of subcortical structures in consciousness has
been further argued based on clinical observations of hydra-
nencephalic children, who are essentially devoid of neocortex and
yet who still demonstrate some behavioral signs of consciousness
(75). Others have attempted to link the arousal related compo-
nents of consciousness with the contents of consciousness by
placing emphasis on the dynamic recurrent activity that occurs in
the thalamus or through the thalamic reticular nucleus when
consciousness is present (83, 84). As such, the PET study showing
that the emergence of consciousness is correlated with increased
Fig. 2. Brain structures functionally related to primitive emotional arousal
and the return of consciousness following sleep or anesthesia. The primitive
emotional response of air hunger shows activations in brainstem and anterior
cingulate regions; thalamic changes are also seen (73). Subjective emotional
arousal activates similar regions in an event-related functional MRI study of
picture viewing. Reproduced with permission from (85). Midline thalamic and
anterior cingulate arousal is seen with PET neuroimaging when consciousness
ﬁrst reemerges following sleep or anesthesia. Reproduced with permission
from (72 and 65). A common brainstem, thalamic, cingulate neuroanatomy
associated with conscious brain activity is seen. Images used with permission.
Table 2. Comparison of neocortex and pallium with respect to requirements for cell assemblies
Requirements for Hebbian cell assembly Structure of mammalian neocortex Structure of avian pallium
Many neurons of the same kind About 85% pyramidal cells High number of multipolar cells
Connections with each other Most synapses are between pyramidal cells Many synapses between multipolar cells
Excitatory connections About 90% of synapses are type 1 (excitatory) Many synapses excitatory
Modiﬁable connections About 75% of synapses are on spines Dendrites are densely spiny
Individual neurons connected to as
many other neurons as possible
About 8,000 synapses per neuron Many synapses per neuron
Distant connections across the network Large amount of white matter Axons more interspersed with neurons
Modiﬁed from (77) with permission from Elsevier.
Mashour and Alkire PNAS
June 18, 2013
activity in “primitive”brain regions may reﬂect an arousal-related
response to the test stimulus itself rather than a direct awareness
of the stimuli that is occurring in the thalamus. In either event,
the data clearly show that the neurocircuitry associated with
arousal is fundamental to consciousness. A further recent study
investigating long-term memory encoding also imaged the neural
correlates of subjective emotional arousal. As shown in Fig. 2, the
neural correlates for awareness of subjective arousal induced by
viewing of emotional stimuli involve the same midbrain arousal
structures seen with activation of primordial emotions (85).
Regarding ontogeny of H. sapiens, peripheral sensory receptors
are thought to be present from 20 wk of gestation in utero. The
developmental anlage of the thalamus is present from around day
22 or 23 postconception, and thalamocortical connections are
thought to be formed by 26 wk of gestation (74). Around the same
time of gestation (25–29 wk), electrical activity from the cerebral
hemispheres shifts from an isolated to a more continuous pattern,
with sleep–wake distinctions appreciable from 30 wk of gestation.
Thus, both the structural and functional prerequisites for con-
sciousness are in place by the third trimester, with implications for
the experience of pain during in utero or neonatal surgery. It is of
interest to note that the third trimester of human development is
thought to be the period in which the maximal proportion of time
spent in REM sleep occurs across the lifespan (86). This ﬁnding
supports the ontogenetic theory of REM sleep as a process of in-
ternally driven neuronal activation that prepares the developing
cortex for the coming inﬂux of sensory stimuli at birth. The theory
of REM sleep as a form of protoconsciousness has recently un-
dergone further elaboration (87).
When Does Consciousness of the Self Arise?
One component of consciousness that seems linked to higher
cognitive abilities is awareness of the self rather than simply
awareness of the environment. One way to test for this possibility
is to use what is known as the mirror self-recognition (MSR) test
(88). In 1970, Gallup found that chimpanzees, but not monkeys,
were able to pass the MSR test (89). This test presupposes that the
experimental subject has sufﬁcient cognitive ability to be aware of
itself as an entity that is distinct from another conspeciﬁc. This
ability then deﬁnes one form of consciousness (i.e., the ability to
have awareness of one’s own awareness or self). In Gallup’s well-
controlled experiment, the animals were ﬁrst allowed ample time
with mirror exposure to allow social responses to their reﬂected
images to diminish greatly. The number of social responses and
the number of self-directed responses were measured before the
animals had a mark covertly placed on their forehead or ear while
they were brieﬂy anesthetized. The animals were then allowed to
recover from anesthesia, and some hours later a mirror was
reintroduced. On seeing themselves in the mirror, the marked
chimpanzees—but not the marked monkeys—exhibited mark-
directed responses by spending time investigating the area of the
mark and examining their ﬁngers after touching the mark. The
ﬁndings led Gallup to conclude “insofar as self-recognition of
one’s mirror image implies a concept of self, these data would
seem to qualify as the ﬁrst experimental demonstration of a self-
concept in a subhuman form.”Regarding the difference between
chimpanzee and monkey, he further concluded, “Our data suggest
that we may have found a qualitative psychological difference
among primates, and that the capacity for self-recognition may
not extend below man and the great apes.”The distinction among
primates suggests that the qualitative nature of the conscious
experience varies greatly across species and the introspective
nature of human consciousness may be evolutionarily quite rare.
The MSR test has now been used to examine the ability of
other species to show evidence of self-awareness. Primates that
have passed the MSR test include chimpanzees, orangutans, and
bonobos. The case for the gorilla is equivocal with mostly neg-
ative ﬁndings; several studies have suggested that more socialized
gorillas might be able to pass the test. Humans begin to develop
a sense of self and pass the MSR test starting around 18 mo of
age, and by 24–36 mo, almost all western children will show a
positive MSR response (90). The distinction between great apes
and monkeys would seem to provide a clear demarcation in the
capacity for consciousness between species. Numerous studies
have supported this demarcation, with multiple failed attempts
to detect self-awareness in monkeys, despite one recent report to
the contrary (91). However, a number of methodological con-
cerns limit enthusiasm for the one contrary study, and overall the
data continue to suggest that macaques do not evidence MSR
behavior (92). In evolutionary terms, if objective evidence of self-
awareness can be taken as evidence for consciousness, then con-
sciousness as it occurs in the primate with their more fully de-
veloped cortex may have evolved ∼5 million years ago, at around
the time when great apes split off from the lesser apes.
Mirror-self-recognition may not be limited to the relatively
big-brained great apes. More recent work with other big-brained
creatures suggest the possibility that dolphins, and at least one
African elephant, may also be capable of this response (93–95).
As apes, elephants, and cetaceans have a very remote common
ancestor, these ﬁndings would seem to suggest that the mental
machinery prerequisite for self-awareness must be at least as old
as the development of the placental divide in mammals (96).
However, we may be able to take this idea on another path in
evolutionary time. As noted, the cognitive abilities of some birds
are now thought to be comparable to the abilities of some pri-
mates (80). Evidence suggests that the brain development of the
bird, which evolved on a different path from mammals, still has a
conceptually similar thalamocortical structure that can be de-
lineated (43). The cognitive abilities of various birds seem to
correlate with the relative size of the analogous avian prefrontal
cortex. Indeed, the crow-like Corvidae (crows, ravens, magpies,
rooks, jackdaws, and jays) appear to have the most advanced be-
havioral repertoire, as well as the largest prefrontal cortex (pal-
lium) (97). Importantly, a recent report shows Magpies (having
a relatively large prefrontal cortex) exhibit behavior consistent
with MSR (98). This ﬁnding, coupled with the current under-
standing of avian neuroanatomy and its well-developed thala-
mocortical structure, suggests that the foundations required for
both consciousness of the world and consciousness of the self may
have formed as early as the amniote radiation (78).
From a cognitive perspective, the meaning of self-awareness
behaviors in a mirror remains somewhat controversial (99). Some
argue that the mirror behavior could be more easily explained
by simple knowledge of one’s body. The neurobiology of having
a body sense is something that is highly linked with a sense of
consciousness (100). Perhaps, as stated by Morin (99), “all an
organism requires to self-recognize is a mental representation of
its own physical self; the organism matches the kinaesthetic
Fig. 3. Schematic showing relative size of frontal lobe across different
species and the potential capacity for anterior–posterior information ﬂow.
The blue areas represent the prefrontal cortex, and the schematic shows
how the prefrontal cortex proportionally increases in size with increasing
brain size across species. Relative brain size is scaled to the human brain.
Modiﬁed from (102) with permission from Elsevier.
www.pnas.org/cgi/doi/10.1073/pnas.1301188110 Mashour and Alkire
representation of the body with the image seen in the mirror and
infers that ‘it’sme’.”A number of other arguments against
overinterpreting MSR have been made, yet despite these relevant
concerns, from an evolutionary point of view the presence or
absence of a MSR response is at least a starting point for con-
sidering what having such a response might mean as a basis for the
evolution of consciousness. The MSR response allows one to
question what is functionally and structurally different about
brains that can self-recognize vs. those that cannot.
Why Is Human Consciousness Unique?
We have argued that the brainstem, diencephalon, and limited
association cortex capable of recurrent processing is consistent
with a core or primitive consciousness. However, what accounts
for the richness of human experience in contrast to those of early
mammals or birds? Drawing on the integrated information the-
ory of consciousness, the evolution of more complex brain net-
works capable of synthesizing the outputs of more functionally
diverse modules would result in a higher capacity for conscious-
ness. Indeed, integration of information appears to correlate
positively with ﬁtness in artiﬁcial agents (animats) (27). It is un-
known in biology, however, whether it is the level or quality of
consciousness that differs across species. Although H. sapiens
may have more advanced cognition, it is difﬁcult to imagine that
a sedentary human has a higher level of consciousness than
a highly alert beast in pursuit of prey; the richness of conscious
experience may be what differs. Alternatively, it is possible that
advanced symbolic processing in human cognition eclipses the
subjective characteristics of experience. In other words, cognition
may be potentially opposed to phenomenal consciousness. De-
spite these considerations, human consciousness—especially the
capacity for self-consciousness and reﬂection/projection in time—
seems unique. Although evidence suggests that the core of con-
sciousness is rooted in phylogenetically older structures such
as the brainstem and diencephalon (75), the evolution of that
which is particular to human consciousness may be more closely
associated with the development of the frontal cortex. The rela-
tive size of the frontal lobes with respect to the total neocortex is
roughly the same in modern humans and great apes, but richer
interconnectivity might account for advanced cognition in H. sa-
piens (101). In particular, directed anterior-to-posterior connec-
tivity has been associated with conscious perception and is
dominant in humans (39) but not in rodents (38, 102) (Fig. 3). It
has been suggested that the afferent information from the
periphery converging at the hub of the posterior parietal cortex
becomes, with the expansion of the frontal cortex, dominated by
a strong anterior-to-posterior reafference (103). Indeed, a recent
neural mass model based on structural connectivity data from
diffusion tensor imaging in humans predicts an information ﬂow
from the frontal to the posterior parietal cortex (104). In essence,
this information ﬂow reversal suggests that human consciousness
is more deﬁned by internal dynamics than external stimuli. This
level of information ﬂow reversal may help explain, in part, those
animals capable of a MSR response. According to one theory,
human consciousness is a closed system or “oneiric”(dream-like)
state that is simply modulated by environmental input (105), a
theory consistent with REM sleep as a building block for human
consciousness. The relative independence from environmental
determination of conscious content would potentially permit
a greater diversity or richness of experience in comparison with
species without dominance of anterior-to-posterior ﬂow. This
independence would also facilitate the projection and simulation
associated with future plans, of clear relevance to survival. It is
important to note, however, that the role of information ﬂow
in consciousness is unclear at this time and requires further
The emergence of consciousness on the evolutionary timeline
has been scientiﬁcally considered at least since the time of
Darwin. The emergence of consciousness from the anesthetized
state may provide a practical and reproducible model for char-
acterizing the real-time evolution of the core neural correlates
required for consciousness of the world and of the self. Using
recent data from general anesthesia in humans, we suggest that
the arousal centers in the brainstem and diencephalon—in con-
junction with even limited neocortical connectivity and recurrent
processing—can result in primitive phenomenal consciousness.
By “reverse engineering,”we postulate that early mammals and
birds possessing these structures (or their equivalents) are capa-
ble of phenomenal consciousness. However, the increased com-
plexity of networks and a functionally dominant prefrontal cortex
in the brain of H. sapiens likely accounts for the unique richness
of the human experience.
ACKNOWLEDGMENTS. G.A.M. is supported by National Institutes of Health
Grant 1R01 GM098578 and the James S. McDonnell Foundation.
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