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COGNITIVE NEUROSCIENCE
AND ANIMAL CONSCIOUSNESS
MATTEO GRASSO
(ROMA TRE UNIVERSITY)
Abstract
The problem of animal consciousness has profound implications on
our concept of nature and of our place in the natural world. In philosophy
of mind and cognitive neuroscience the problem of animal consciousness
raises two main questions (Velmans, 2007): the distribution question (are
there conscious animals beside humans?) and the phenomenological
question (what is it like to be a non-human animal?).
In order to answer these questions, many approaches take into account
similarities and dissimilarities in animal and human behaviour, e.g. the use
of language or tools and self-recognition in a mirror (Allen and Bekoff,
2007); however, behavioural arguments do not seem to be conclusive
(Baars, 2005). Cognitive neuroscience is providing comparative data on
structural and functional similarities, respectively called homologies and
analogies. Many experimental results suggest that the thalamocortical
system is essential for consciousness (Edelman and Tononi, 2000; Tononi,
2008). The argument from homology states that the general structure of
the thalamocortical system remained the same in the last 100-200 million
years, because it is neuroanatomically similar in all the present and past
mammals, and it did not change much during phylogeny (Allen and
Bekoff, 2007). The argument from analogy states that the key functional
processes correlated with consciousness in humans are also present in all
other mammals and many other animals (Baars, 2005). These processes
are information integration through effective cortical connectivity
(Massimini et al., 2005; Rosanova et al., 2012), and elaboration of
information at a global level (Dehaene and Changeux, 2011).
On this basis, the Cambridge Declaration on Consciousness stated
that all mammals, birds, and many other animals (such as octopuses)
possess the neurological substrates of consciousness (Low et al., 2012).
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Conscious experience is private (Chalmers, 1995; Nagel, 1974), therefore
the answer to the phenomenological question may be impossible.
Nevertheless, cognitive neuroscience may provide an answer to the
distribution question, showing that conscious experience is not limited to
humans since it is a major biological adaptation going back millions of
years.
1. Two Questions on Animal Consciousness
Consciousness is the most intimate and patent aspect of the
experiences we undergo daily. From when we wake up to when, lying in
bed, our senses are blurred and we sink into sleep, consciousness is a
matter of fact, and so it seems perfectly obvious to us. In our lives we are
spontaneously able to establish whether other people are conscious or not:
we recognize when someone faints from fear, we are aware of pathological
conditions characterized by the loss of consciousness such as coma, and
we rely on the anaesthetist before an important operation so that the drugs
administered erase, together with consciousness, all the pain and the
unpleasant memories of the surgery.
Despite this daily competence, it is hard to explain the criteria we use
to determine whether an individual is actually conscious or not. Most of
the times we just have to rely on observed behaviour: individuals who
interact with the exterior environment and with other people are evidently
conscious, especially if they are able to react consistently to stimulations
and respond to our questions in a meaningful way. However, an objective
judgment given from an external point of view, from the third person, is
not enough: would we say that sleepwalkers are conscious just because
they interact with the external environment? In an intuitive and simplistic
way, we could say that individuals are conscious only if it is something to
be them. Given that during deep dreamless sleep, or under general
anaesthesia, we do not feel anything, we could say that in such cases
consciousness disappears completely.
However, the ability to evaluate consciousness might go beyond the
limits of our own species: are animals such as dogs and cats conscious,
too? They show complex behaviour, we empathize with them, we believe
they understand our emotions and our feelings and many times we even
talk to them. Are animals phylogenetically more distant from us (such as
birds and fishes) conscious as well? Where does the boundary lie between
animals that are conscious and animals that are not? With respect to these
questions, our intuitions are useless and unfit, and they find us totally
unprepared and unable to provide even the slightest response. Precisely
Cognitive Neuroscience and Animal Consciousness
184
because of the elusiveness of consciousness, even scientists and philosophers
are in deep water when considering these issues.
The problem of animal consciousness has profound implications for
the concept of nature and the place of man within it. For a long time,
anthropocentrism has been characterizing the view that humankind has of
itself as a privileged species at the top of the so-called Scala naturae, as
was considered to be the only being endowed with intellect, soul or simply
mind and consciousness.
The problem of animal consciousness comes up again, now more than
ever, in the philosophical and scientific debate, bringing along several
implications about the centrality of humankind in the natural world as well
as ethical implications. In fact, many animal species are used in research
and industry, and many of them are subject to intensive farming. The
assumption that our ethical obligations towards animals depend on their
mental life is quite common and well-grounded in intuition (Farah 2008),
and the ethical issue concerning animals is of primary importance. In fact,
the rejection of the hypothesis of animal consciousness seems less and less
grounded, given the increasing amount of scientific models of affective
and emotional experiences both in humans and other animals (Panksepp
2005).
In recent years, two fundamental questions about animal consciousness
have been at the centre of a big debate, involving both philosophy of mind
and cognitive neuroscience (Allen and Beckoff 2007). The first is the so-
called distribution question (DQ):
(DQ): Are there conscious animals beside humans?
Many animal species share the ability to respond to environmental
stimuli with intelligent behaviour, and the organisms phylogenetically
closer to Homo sapiens share with us several anatomical structures.
However, there is no objective criterion available for determining with
certainty whether there are other conscious animals besides humans.
Consciousness might in fact be a common feature of many species,
including the class of mammals, or the entire group of vertebrates;
nevertheless, without a reliable criterion we cannot establish any useful
test to distinguish between conscious and unconscious organisms.
Being conscious is not just being awake and reactive, or being able to
respond to environmental stimuli and show intelligent behaviour. Being
conscious also means having experience of the world, of the actual shape
of a flower, the colours in the sky, the smells and flavours of food; being
conscious means having desires, feeling pain from the wounds, feeling
fear of predators, and so on. Thus, there is a second important question on
Matteo Grasso 185
animal consciousness that focuses on the qualitative aspects of conscious
experience and is expressed in the form of the so-called phenomenological
question (PQ):
(PQ): Can we know what, if anything, the experiences of those animals are
like?
Many philosophers think that consciousness is the last surviving
mystery, and that science cannot face up to the problem of consciousness
because of its subjective and phenomenal aspects. According to Chalmers
(1995), conscious experience constitutes the very and only hard problem
that science has to tackle. Both the hard problem and the PQ are based on
the concept of phenomenal consciousness, introduced by Ned Block
(1995) and widely debated in the philosophy of mind. This concept refers
to the subjective and qualitative nature of each experiential state of
consciousness, whether it belongs to humans or not. What does a wasp feel
when glancing at the colours of a flower? What does a cow experience
while looking into the eyes of the farmer who milks her daily? Can we
make a comparison between the conscious and subjective experience of
being a man with the experience of being another animal?
These questions are loaded with both metaphysical and ethical
implications, and these issues constitute the core of deep philosophical
reflections. The DQ relates to the issue of the centrality and superiority of
mankind in the natural world at its core and the question admits two
contrasting answers: Yes, there are conscious animals besides humans or
No, there are not.
Two types of theories about the distribution of consciousness in nature
have been proposed in order to answer the DQ (Velmans 2007), namely
discontinuity and continuity theories. Discontinuity theories state that
consciousness emerged at a certain stage of the phylogeny. The models
that equate this stage with the evolution of the genus Homo usually reply
negatively, claiming that only humans are endowed with consciousness
and that the distribution of consciousness is discontinuous, since it belongs
only to them. The models which instead place such a gap elsewhere are
inclined to reply in a positive way, claiming that in nature there are many
living organisms endowed with consciousness. According to this view,
this phenomenon has emerged at a specific stage of phylogeny and it is a
shared feature of either the entire taxon of vertebrates, or the sole group of
mammals, or the primates alone, depending on the particular view. In
general, discontinuity theories share a vision of nature that presents jumps
and in which the living organisms endowed with consciousness are sharply
divided from all the others. As we will see in the following paragraphs,
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186
many discontinuity models have recently been proposed.
On the contrary, continuity theories always reply Yes, there are
conscious animals besides humans; indeed, they think there are plenty of
them. Continuity theories argue that consciousness is a property that has
always characterized living beings, and that it is distributed in different
degrees throughout the natural world. These theories often embrace a form
of panpsychism, arguing that consciousness is a fundamental property that
characterizes, to a certain extent, even matter itself, albeit at low and
irrelevant levels, and that it co-evolves in complexity with matter and its
aggregates (Chalmers 1995; Velmans 2007; Whitehead 1929).
Among the many proposals aimed at addressing the distribution
question, some are based on the identification of similarities and
dissimilarities in the behaviour of humans and other animals, but
behavioural observations do not seem to be a reliable and satisfactory
criterion (Baars 2005). However, the two questions about animal
consciousness have caused even more discussion since additional non-
behavioural arguments appeared in the scientific and philosophical debate.
In recent years, cognitive neuroscience has been shedding light on the
neural structures essential for consciousness in humans, raising several
questions about the distribution of consciousness in nature and strongly
influencing the debate on animal consciousness. A new neuroscientific
line of argument is based on the similarities found at the neural level in
species different from Homo sapiens, and it is deeply connected with the
identification of those structures and processes that constitute the neural
substrate of consciousness in human beings.
In this article, I will firstly discuss the most important examples of
behavioural arguments and I will argue that such arguments are
unsatisfactory. Then, I will show how cognitive neuroscience has
contributed so far to the study of animal consciousness, and I will show
the conclusions that can be drawn in the light of these findings. Finally, I
will argue that cognitive neuroscience is the only reliable base to answer
philosophical questions such as the distribution question. Nevertheless,
neuroscientific progress cannot lead to the solution of philosophical issues
related to subjective conscious experience, since it cannot contribute to the
formulation of an answer to the phenomenological question.
2. From Behaviour to Consciousness
Whenever we have to give a reason why we consider a human
conscious as opposed to, say, a computer, we most likely begin with
noticing the following: a human being is capable of complex behaviour
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that goes well beyond the mechanical and automatic processes a computer
is able to carry out with flawless precision. The observed behaviour is one
of the most important criteria, so much that artificial intelligence research,
since its origins, was based on the idea that building a computer able to
implement typically human behaviours such as language or reasoning
would correspond to recreating mental processes similar to those that
occur in the human brain. Indeed, one of the fathers of artificial
intelligence, Alan Turing, considered the behavioural criterion as the most
reliable basis for developing a test of machine intelligence, now known as
the Turing test (Turing 1950). In the same way, the debate has always
been focused primarily on behavioural observations also with respect to
the issue of animal consciousness, and many arguments based on the
similarities between the behaviour of humans and other animals have been
proposed (Allen and Beckoff 2007).
One of the most evident abilities that characterize humans is the use of
language. Our species, through the use of historical-natural languages, has
been able to communicate and build the characteristic complex network of
social ties. Some philosophers, such as Descartes, argued that the use of
articulate languages is a clear sign of the ability to reason, and therefore
constitutes the basis for inferring the presence of consciousness in other
living beings (Descartes 1984-91). Humans, however, are not the only
animals that use language. There have been many instances of non-human
animals able to use a language in order to communicate. Professor Irene
Pepperberg spent decades studying the linguistic skills of an especially
talented African grey parrot (Psittacus erithacus). The grey parrot Alex
showed many similarities with the use of language typical of human
beings, in stark contrast to the Cartesian idea that animals are not equipped
with language, or are only capable of a very limited use of it. Alex had a
vocabulary of a hundred and fifty words (similar to that of a two-year old
child), he could identify fifty different objects and recognize quantities up
to six, he could distinguish seven colours and five shapes, he understood
the concepts of zero and said I want to go back to my cage when he was
tired (Pepperberg 2002). Linguistic skills have also been found in many
other animal species besides African grey parrots, in the form of the
capacity to use a modified sign language or symbols of the Yerkes
Laboratory keyboard system (chimpanzees, bonobos), or alarm calls
(lemurs, vervet monkeys, social mongooses and prairie dogs) (Griffin and
Speck 2004).
The use of language, although largely correlated with the complex
cognitive processes Homo sapiens is capable of, might not be certain
evidence of the presence of consciousness. In fact, discussing the example
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188
of parrots, Descartes (1984-91) argued that any process put in place by
these and other animals is in principle conceivable as purely mechanical.
Parrots, in this case, could talk without being aware of it, and this would
also explain the limited use of language that distinguishes all other species
compared to humans.
Besides the use of language, the use of tools is often considered a
second indication of intelligence and complex mental faculties. Once
again, the animal kingdom presents many examples of species that show this
capability. Among the various species, certain crows represent perhaps the
most interesting example. New Caledonian crows (Corvus moneduloides)
show the ability of crafting tools, such as wooden hooks, that they
subsequently use to probe for invertebrates in crevices. In several
experiments it was observed that these crows, when placed in proximity of
a 30-cm-long cylindrical container with a single opening and containing a
favourite food, are able to immediately retrieve one of the sticks available
in the cage and, holding it with their beak, slide it into the cylindrical tube
to extract the food (Hunt and Gray 2004). In nature, the crows insert sticks
into cavities and drag out the preys that would be difficult or impossible to
flush out otherwise. If faced with a vertical cylinder containing a bucket of
seeds, such crows are able to grasp with their beak a metal stick, bend it
leveraging on one end so as to fabricate a hook, and use it to extract the
bucket of seeds from the cylinder (Weir, Chappell and Kacelnik 2002).
Despite the ability to communicate and use languages or tools, further
types of behaviour might seem to be solid evidence of the presence of
consciousness in non-human animals. Less than fifty years ago, in order to
ascertain the presence of self-awareness and meta-consciousness,
Professor Gordon Gallup devised the so-called mirror test. It has long
been known that species phylogenetically close to Homo sapiens, such as
chimpanzees, are very attracted by the use of mirrors, and contemplate
themselves in their own reflected image. Starting from this evidence,
Gallup has developed the mirror test in order to determine whether these
animals are actually able to recognize themselves in the reflected image, or
they are interested in it only because they recognize the shape of one of
their own kind. For this purpose, Gallup put several chimpanzees in front
of a mirror, leaving them contemplating their own reflected image for a
few days. After an initial period in which the animals responded by
attacking the image or getting frightened, they eventually got used to it
and began to simply contemplate the reflections in the mirror. At that
point, Gallup marked the bodies of the animals with odourless paint , in a
place visible only in the mirror. The animals showed evidence of
understanding that the stain was on their own body, and would in fact turn
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the stained part of the body towards the mirror for a better look and
inspected the same body part with a limb while looking in the mirror
(Gallup 1970). According to Gallup, mirror self-recognition is an indicator
of self-awareness. Furthermore, he claims that the ability to infer the
existence of other individuals mental states (namely, having a theory of
mind) is a by-product of self-awareness. He describes the connection
between self-awareness and theory of mind by saying that, being self-
aware, an individual is in a position to use his own mental experience to
infer and model the existence of comparable mental and intentional
processes in others (Gallup et al. 2002).
It is clear that much additional work will be required before a complete
report. However, a list of the animals that have passed the mirror test so
far includes humans (from the age of 18 months) as well as all the great
apes such as chimpanzees, gorillas, bonobos and orangutans (Miller 2009),
some marine mammals such as bottlenose dolphins (Marten and Psarakos
1995) and orca whales (Delfour and Marten 2001), but also elephants
(Plotnik, de Waal and Reiss 2006) and European magpies (Prior, Schwarz
and Güntürkün 2008).
Thus, many approaches take into account similarities and dissimilarities
in animal and human behaviour. Nonetheless, behavioural arguments do
not seem to be conclusive (Baars 2005). Even though behaviour might
appear as a reliable criterion for assessing the state of consciousness in
humans as well, recent developments in cognitive neuroscience have
shown that there is no substantial proof. For instance, neurology and coma
science have provided many examples in which the assessment of the level
of consciousness is a puzzling clinical issue. This is the case of non-
communicative patients who, despite being perfectly aware, are unable to
prove it by means of any observable behaviour. Indeed, neuroscience has
recently started providing methods and tools for assessing consciousness
that are not behaviour-based (Rosanova et al. 2012). These tools are
proving their usefulness in the diagnosis and treatment of disorders of
consciousness (and related conditions) such as the locked-in syndrome,
and for the reasons outlined so far they might be very useful in the study
of animal consciousness as well.
3. Neuroanatomy and Neurophysiology
of Human Consciousness
The study of animal consciousness is the centre of a renewed interest
because of the appearance of a new series of arguments. These arguments
are based not on the observed behaviour, but on the animals brain
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190
structures and processes, which are similar to human ones, that can be
investigated using the tools of neuroscience. Cognitive neuroscience is
gradually leading to a better understanding of the neural correlates of
consciousness in humans and, in doing so, it is offering at the same time
the opportunity to start investigating consciousness in other animals on a
completely new basis.
In recent years, several theoretical and experimental models attempted
to identify the structures and processes responsible for consciousness in
humans. On the one hand, it is generally believed that the basic structure
for the emergence of consciousness is mainly the thalamocortical system
as a whole, with a specifically important role played by the prefrontal,
cingulate and parietal cortices (Edelman and Tononi 2000; Laureys and
Tononi 2009). On the other hand, besides anatomical structures, the
fundamental processes of consciousness are cortical connectivity through
information integration (Tononi 2008; Edelman and Seth 2009) and
elaboration of information shared and processed at a global level (Dehaene
and Changeux 2011; Tononi and Koch 2008).
The 100 billion neurons that constitute the central nervous system are
organized into different structures that are important for the emergence of
consciousness. Considering only the cerebral mass and the number of
neurons, for example, one could think that consciousness emerges from
the interaction of an exorbitant number of cells that are able to exchange
electrical signals by means of an even greater number of intricate synaptic
connections. However, extensive neurological evidence has shown that
consciousness does not depend exclusively on the number of neurons. The
100 billion neurons contained in the central nervous system are divided
into two distinguishable structures: the thalamocortical system and the
cerebellum. The cerebellum is a single body with a complex structure and
consists of about 70 billion neurons, while the thalamocortical system is
composed of about 21 billion nerve cells (Pakkenberg et al. 2003; Llinàs,
Walton and Lang 2004). Despite their similarity, these two structures
contribute in a very different way to consciousness because, contrary to
the cerebellum, the thalamocortical system is crucial in supporting
consciousness (Edelman and Tononi 2000). The thalamocortical system is
composed of the thalamus, a deep structure located in the diencephalon,
and the cerebral cortex, the thin layer of neurons that constitutes the outer
(and most recent) part of the telencephalon in vertebrates. This structure is
considered responsible for complex cognitive processes such as memory,
perception, thought, and language. As many cases studied by clinical
neuropsychology demonstrate, injuries to this structure of the central
nervous system can cause the loss of cognitive functions such as
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perceptive abilities, memory, thinking and reasoning, as well as the
complete loss of consciousness (Laureys and Tononi 2009). Even a slight
damage to some areas of the thalamocortical system (such as the brainstem
or the ascending reticular activating system) can cause a total loss of
consciousness, leading the subject into a state of coma, vegetative state or
even brain death (Vincent 2000).
The cerebellum too is responsible for important functions, such as
motion control and motor learning, but this structure does not seem to play
any significant role with respect to conscious experience. In fact, as a
result of cerebellectomy, a surgery which consists in the total removal of
the cerebellum, patients show serious deficits in posture and gait control,
linked to the impaired control of limbs and eye movements (cerebellar
ataxia); however, none of the cognitive functions seem to be damaged in
these patients (Tononi 2008). In fact, the cerebral cortex and the cerebellar
cortex have a very different structural organization: the modules of the
cerebral cortex, as highly specialized, are abundantly connected to each
other, while individual modules in the cerebellar cortex tend to be
activated independently of one another, with little long-range interaction
possible between distant modules (Tononi 2004, 2008). This shows that
the integration of information through a complex network of long-range
connections is fundamental for the emergence of consciousness.
Recently, Stanislas Dehaene proposed the Global Neuronal
Workspace model in order to explain which fundamental property is
responsible for the emergence of consciousness from the thalamocortical
system. Dehaene and his colleagues argue that the thalamocortical system
is responsible for the emergence of consciousness as composed of a
particular structure, the global neuronal workspace, consisting in a
group of cortical pyramidal neurons with excitatory function and with
long-range cross-cortical axons. A high density of this cell type is located
in the prefrontal, cingulate, and parietal cortices, and, according to this
model, together they would form a neuronal workspace connecting a
large number of peripheral processing systems and specialized modules,
which otherwise always work isolated and on a subconscious level
(Dehaene and Changeux 2011). In this model, the prefrontal cortex is a
root node of a global network formed by long-distance synaptic
connections. This assumption is confirmed by the fact that the prefrontal
cortex is connected with a number of very different sensory areas through
cortico-cortical connections, and this massive two-ways connectivity
justifies the important role played by this particular structure in the
hypothesis of a global workspace connecting many areas of the
thalamocortical system and supporting consciousness.
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192
There is very strong evidence that the thalamocortical system supports
consciousness. However, although the presence of such brain structures is
a necessary condition, it is not yet sufficient in attributing consciousness to
a subject. We are witnesses to the fact that every night consciousness
disappears when we fall asleep in a dreamless sleep, but of course the
anatomy of our nervous system does not change from day to night. The
changes responsible for this daily loss of consciousness are instead due to
the availability of neurotransmitters and the particular activity pattern of
the billions of neurons that form the thalamocortical system. As shown by
electroencephalographic (EEG) measurements, during stage 4 of NREM
sleep the firing rate of many cortical and sub-cortical neurons is
characterized by oscillatory synchrony and bistability: neuromodulatory
changes (e.g. low acetylcholine) trigger a modification in the intrinsic and
synaptic conductance, therefore cortical neurons enter every few hundred
milliseconds in a hyperpolarized down-state and cannot sustain firing for a
short period of time. Shortly afterward, they inevitably return to a
depolarized up-state and start their action potential activity again (Steriade,
Timofeev and Grenier 2001). According to Giulio Tononis Integrated
Information Theory, consciousness fades in deep sleep because of a
decrease in the capacity to integrate information that characterizes the
whole thalamocortical system in this state. This capacity is greatly reduced
in deep NREM sleep because the thalamocortical system breaks down into
causally independent modules and shrinks its repertoire of possible
responses, therefore losing effective cortical connectivity and the
capability to elaborate high amounts of information at a global level
(Tononi and Massimini 2008; Massimini et al. 2005).
Moreover, the importance of the thalamocortical system is also shown
by the fact that several consciousness disorders are due to neurological
damage to this structure. The most common disorders that produce at least
transient coma are structural brain lesions (cortical or white matter
damage, and brainstem lesions), metabolic and nutritional disorders,
exogenous toxins, central nervous system infections such as septic illness,
seizures, temperature-related disorders (hypothermia or hyperthermia), and
trauma (Laureys and Tononi 2009). All these injuries or conditions
interfere with the ascending reticular activating system (ARAS). The
ARAS plays a central role in disorders of consciousness because it is the
system responsible for the arousal function. As it is represented by
structures in the brainstem, the diencephalon and projections to the
cerebral cortex (Vincent 2000), the state of unarousable unconsciousness
named coma is the effect of an impairment in this system (Laureys and
Tononi 2009). In addition, recent studies show impaired functional
Matteo Grasso 193
connections between distant cortical areas and between the thalami and the
cortex in vegetative patients (Laureys et al. 2002). More importantly, these
studies suggest that a restoration of this cortico-thalamo-cortical interaction
causes a recovery of cortical effective connectivity (Rosanova et al. 2012)
and therefore the recovery of consciousness (Laureys et al. 2000).
Given the base these findings constitute, is it possible to deal with the
problem of determining the distribution of consciousness in nature? How
confident can we be in determining, on the chronological and phylogenetic
tree of life, the position of the line that separates conscious organisms
from unconscious ones?
4. Homologies and Analogies
Cognitive neuroscientists have provided comparative data on structural
and functional similarities between different species, respectively called
homologies and analogies. Homologies are phenotypical characters,
namely bodily structures, similar in different species because they were
inherited from a common ancestor possessing those characters. Analogies
are phenotypical characters similar in different species because of
convergent evolution instead of common ancestry. These characters
evolved independently but are thought to be analogous for the similar
function they play and were selected for.
The arguments based on neural homologies state that the general
structure of the thalamocortical system remained the same in the last few
hundred million years, for it is anatomically similar in all currently
existing and past mammals and did not change much during phylogeny.
Moreover, these arguments state that the key functional processes
correlated with consciousness in humans are also present in all other
mammals (Edelman, Baars and Seth 2005). According to this hypothesis,
consciousness is a biological adaptation dating back many millions of
years (Baars 2005).
Even on the basis of neuroscientific arguments, however, it is still very
hard to formulate a precise answer to the question about the distribution of
consciousness in the natural world. To this day, many hypotheses have
been proposed about consciousness in non-human animals, covering
different taxa such as mammals, vertebrates and invertebrates as well.
According to Baars (2005), the comparison between the thalamocortical
structures of man and those of other mammals suggests the possibility of
attributing consciousness to this whole category of living organisms: all
mammals, in fact, have a highly developed thalamocortical system. The
study of cranial fossil remains and gene conservation across species
Cognitive Neuroscience and Animal Consciousness
194
suggests, moreover, that the fundamental structures of the thalamocortical
system have not undergone major changes over the last 100-200 million
years.
Furthermore, it is possible to detect in all mammals the same EEG
activation patterns observed in man, so that the results of EEG studies on
mammals are often directly applied to humans. During the waking state,
the EEG of all mammals shows low-voltage, fast and asynchronous neural
activity throughout the whole thalamocortical system. On the contrary,
during deep sleep the EEG reveals slow, synchronous and high-voltage
activity. Moreover, the wake-sleep cycle has many similarities among all
mammals: with a few exceptions such as whales, most mammals have
both NREM sleep and REM sleepa stage of sleep characterized by the
rapid and random movement of the eyes and the higher presence of
dreams. The variation of electrical brain activity in the transition between
waking and sleep states is one of the features that humans and other
mammals have in common: in humans synchronous oscillatory activity
corresponds to the lack of consciousness, as shown during deep sleep,
general anaesthesia and in other pathological conditions such as coma and
epileptic seizures, and this kind of activity contrasts sharply with the
presence of consciousness during the waking state. The distinction
between waking and sleep therefore constitutes one of the most reliable
criteria to confirm the presence or absence of consciousness in humans
and other animals (Baars 2005).
Homologies are necessarily remoter in non-mammals, which do not
share the mammalian complex thalamocortical system. Avian species
exhibit a broad range of complex behaviours, like the use of tools by New
Caledonian crows, but what do neuroanatomical studies tell us about it?
The overall organization of the central nervous system can be traced back
to some 520 million years ago and it seems a common feature of some
lower vertebrates such as reptiles, as well as birds and mammals (Smith
1999). Birds have anatomical structures that represent homologies and
analogies compared to the thalamus and to the cerebral cortex of
mammals: in the avian dorsal pallium, for example, the somatomotor
circuitry seems a clear homology of the mammalian basal ganglia-cortico-
thalamic loop (Medina and Reiner 2000). Moreover, they have waking
EEG patterns similar to those detectable in mammals during the waking
state (Edelman et al. 2005). Nevertheless, EEG patterns of avians during
sleep are different from those of mammals, although their sleep is
characterized by both REM and NREM sleep (Ayala-Guerrero 1989).
Since reptiles show less homologies and analogies with brain structures
and processes that are fundamental for consciousness in humans and other
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mammals, it is unclear whether reptiles are capable of conscious
awareness. However, mammalian and avian species show homologous
structures or similar analogous arrangements, suggesting the hypothesis
that consciousness emerged approximately 300 million years ago,
probably twice and in an independent way, after the divergence of the two
reptilian lines that led alternatively to birds and mammals (Kardong 1995;
Edelman et al. 2005).
Further studies about the possibility of attributing at least primary
consciousness to other organisms belonging to invertebrate species are
currently being discussed, and many of them focus on cephalopods like the
octopus (Merker 2005). Octopuses (Octopus vulgaris) possess refined
cognitive capabilities. They show the ability of classifying different
shaped objects in the same manner as vertebrates such as rats do. They
show also memory, learning and complex decision-making skills.
Cephalopods like the octopus have complex nervous systems similar to
those of some vertebrates, at least with respect to the number of
constituent neurons alone: the relative brain size of many cephalopods
exceeds that of many lower vertebrates (Hanlon and Messenger 2002).
Nevertheless, contrary to birds, cephalopods show a different organization
of the nervous system that poses many problems in identifying the
necessary structures underlying consciousness (Edelman et al. 2005).
Moreover, a significant fact is that many cephalopods show EEG patterns
akin to those present in awake and conscious vertebrates (Bullock and
Budelmann 1991), and they are the only invertebrates in which this was
demonstrated, besides fruit flies.
So far, experimental evidence has been insufficient to draw any
definitive answer to the DQ. However, as we increase our knowledge we
may be able to make more profound and reliable predictions that apply not
only to some birds and reptiles, but also to large-brained invertebrates and
possibly to many other species (Seth and Baars 2005).
5. The Cambridge Declaration on Consciousness
Recently, the hypothesis of animal consciousness has given rise to a
huge debate. Philosophers and scientists of every background and
orientation are facing up to the related theoretical issues, and they are
discussing the experimental evidence that has gradually accumulated.
However, the problem of animal consciousness might not remain
unresolved. In fact, as I showed so far in this paper, consciousness studies
have increased dramatically over the past few decades. A huge amount of
brand new data is available today and might shape reflection on this issue.
Cognitive Neuroscience and Animal Consciousness
196
2012 was undeniably an important year for the studies on animal
consciousness because it witnessed an important event. A group of eminent
scientists from different countries met and signed a document of central
importance for the animal consciousness debate: the Cambridge Declaration
on Consciousness (Low et al. 2012). The team of scientists included
neuroscientists, neurophysiologists, neuroanatomists, neuropharmacologists
and computational neuroscientists. The Declaration was proclaimed in
Cambridge, UK, on July 7, 2012, at the Francis Crick Memorial Conference
on Consciousness in Human and Non-Human Animals, at the Churchill
College, University of Cambridge, by Philip Low, David Edelman and
Christof Koch. In this two-page document, these prominent neuroscientists
summarized many experimental observations and made several assertions
that can be now unequivocally claimed about the matter of animal
consciousness.
Firstly, the Declaration states that new techniques are available for the
study of the neural correlates of consciousness in humans and non-human
animals, and these studies have shown that it is possible to identify
homologous brain circuits whose activity correlates with conscious
experience, and which can be selectively facilitated or disrupted to
determine whether they are necessary for conscious experience or not.
According to the authors, a lot of evidence indicates that non-human
animals possess the neuroanatomical, neurochemical and neurophysiological
substrates that sustain consciousness and the ability to carry on complex
intentional behaviours.
The neural circuits that support attention, the sleep-wake cycle and
decision-making are found in many animals, such as insects and
cephalopods, and date back to the invertebrate radiation. Birds, in particular,
represent a remarkable case of parallel evolution of consciousness, because
they show evidence of human-like levels of consciousness in their
behaviour, supported by strong similarities in the neurophysiological
processes and neuroanatomical structures of their nervous system.
In conclusion, the subscribers of the Cambridge Declaration on
Consciousness clearly state the following:
Convergent evidence indicates that non-human animals have the
neuroanatomical, neurochemical, and neurophysiological substrates of
conscious states along with the capacity to exhibit intentional behaviors.
Consequently, the weight of evidence indicates that humans are not unique
in possessing the neurological substrates that generate consciousness. Non-
human animals, including all mammals and birds, and many other
creatures, including octopuses, also possess these neurological substrates.
(Low et al. 2012, 2).
Matteo Grasso 197
6. What Is It Like To Be a Bat?
The phenomenological question focuses on the concept of phenomenal
consciousness, namely the subjective and qualitative aspects of conscious
experience, on the first-person point of view that we would not ascribe,
for example, to a robot only because it seems capable of complex
calculations and responses. What is it like to be a non-human animal? It is
hard to say, first of all because animals do not talk and cannot tell us, or at
least because we do not know how to communicate with them. In 1974
Thomas Nagel put the emphasis on this aspect in his famous article What
is it like to be a bat?, in which he argued that conscious experience is
different from every other property of the natural world because it is
private. According to the author, even granting the fact that other animals
might feel something, we will never know what it is like to be one of
them. Indeed, even if one could imagine it, he would know what it is like
to be a bat for a man, and not what it is like to be a bat for a bat (Nagel
1974). The privateness of others mental experience outlines a limit so
clear and insurmountable that it could cast doubts on the very fact that it is
really something to be another animal.
However, this privateness does not only characterize the mental states
of non-human animals, but also the conscious experience of our own
fellow conspecifics. The philosophical problem of other minds leads to
the sceptical conclusion that, by observing the behaviour of other human
beings, we could never conclude that they, too, have a conscious mind
(Nagel 1986). Only the subject himself can be sure of possessing a mind
and of being conscious, as he alone has privileged access and experiences
first-hand the fact of being conscious. For this reason, the privateness of
conscious experience and the problem of other minds lead to two
alternative ways to answer the question: the first is the sceptical and
solipsistic conclusion that each subject believes to be the only one having
for sure a conscious mind, while the second consists instead on relying on
an inference to the best explanation admitting that, despite the
unbridgeable gap between the first and the third person point of view,
there are good reasons to believe that there are other conscious minds as
well besides that of the subject himself.
If you accept the second view, and this is the most interesting point,
the conscious experience of other humans would not seem more accessible
than that of non-human animals. Therefore, the reasons we have to infer
that our fellow humans are conscious, since they share the same
anatomical structures and implement the same types of behaviour,
constitute the basis for inferring that many non-human animals are equally
Cognitive Neuroscience and Animal Consciousness
198
conscious. Thus, the privateness of conscious experience does not limit the
possibility of answering the question about the distribution of
consciousness in the natural world.
It is clear that much additional work will be required in order to
identify which (and to what extent) non-human animals are conscious, but
it seems that the distribution question will have in any case a positive
answer. However, the privateness of conscious experience will probably
remain an insurmountable limit to our understanding of what it is like to
be such other animals, leaving the phenomenological question completely
unanswered.
7. Conclusions
The problem of animal consciousness is perhaps one of the most
relevant issues that philosophy of mind and cognitive neuroscience are
facing today. The new research paradigm based on neuroscience has
achieved important results in just a few decades, and this seems to be just
the beginning of an era full of new and astonishing results. Cognitive
neuroscience is broadening our understanding of the neural basis of
consciousness in man, through the study of consciousness in normal
conditions as waking and sleeping, and it is shedding light on which
mechanisms regulate its disappearance in pathological conditions such as
coma, providing a basis to improve the diagnostic process and the clinical
treatment of such diseases and conditions.
In the past, the debate on animal consciousness was mainly based on
behavioural observations, and many arguments for or against animal
consciousness were grounded in behavioural similarities and dissimilarities
of other animals with respect to human beings. As we have seen, human
consciousness studies today, constitute the basis for a new type of
arguments, based no longer on behavioural observation but on the direct
comparison between different kinds of anatomical structures and brain
processes that, in humans, are known to give rise to consciousness. The
neuroscientific research of interspecific homologies and analogies is
suggesting that man is not the only animal endowed with consciousness.
The basic structure for its emergence, i.e. the thalamocortical system, was
already present for about 150-200 million years before Homo sapiens
appeared, and characterizes the entire class of mammals. Moreover, in
many animals we can find the same brain processes that are essential for
consciousness in man (such as the presence of electrical brain activity in
distinct stages of waking, NREM and REM sleep), and this evidence
suggests that animals distant from man from a phylogenetic point of view,
Matteo Grasso 199
like birds, or even invertebrates such as cephalopods, possess at least a
primary form of consciousness.
Given that conscious experience is private, we cannot explain what it is
like to be another animal. Therefore, answering to the phenomenological
question may be impossible in principle. Nevertheless, cognitive
neuroscience may provide an answer to the distribution question, showing
that conscious experience is not limited to humans but is a major
biological adaptation going back many millions of years. The further
progress of neuroscience will clarify how wide we should consider the
class of living organisms endowed with consciousness. However, at the
moment the evidence is strong enough to consider all mammals and some
vertebrates such as birds as fully belonging to that class. Only future
research and the synergy between philosophy and cognitive neuroscience
will eventually explain the evolutionary history of consciousness, showing
a discontinuity in its distribution, if it emerged at a precise stage of
phylogeny, or showing its continuity across the natural world. Therefore,
from now on, cognitive neuroscience will probably represent the base for
the debate on animal consciousness. As the Cambridge Declaration of
Consciousness argues, many conclusions about animal consciousness can
already be stated unequivocally, and further data and experimental
evidence will foster even moreand on a scientific basisthe ethical and
philosophical debate on the relationship between humans and other
animals.
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