Content uploaded by Shreejata Gupta
Author content
All content in this area was uploaded by Shreejata Gupta on Sep 18, 2015
Content may be subject to copyright.
Chapter 9
Executive Functions as a Path to Understanding
Nonhuman Consciousness: Looking Under
the Light
Shreejata Gupta and Anindya Sinha
9.1 Introduction
The human mind has traditionally been considered unique, surpassing, both
qualitatively and quantitatively, the mental capacities of other animals. In this
sense, the cognitive abilities of humans, unlike the anatomical, morphological
and physiological attributes of the species, arguably fall out of the conventional
evolutionary continuity observed across the animal kingdom (but see Sinha 1999a).
This discrepancy, however, is possibly a direct result of the perspective most widely
adopted in comparative cognitive science. More often than not, we define complex
cognitive behaviours in terms of those expressed in humans, and consequently,
our attempts to establish exactly the same structural and functional attributes of
cognitive systems in other species fail. Such a top-down approach has, therefore,
been unable to provide any meaningful insights in our evolutionary understanding
of cognition.
Consciousness is an excellent example of this kind of a problem. Humans are
generally considered unique in being conscious, and our familiar top-down approach
suggests an absence of this apparently unusual attribute in nonhuman animals.
In this chapter, we argue that consciousness, perhaps, is a process akin to any
other behavioural manifestation and is probably not an indivisible entity, as was
S. Gupta ()
School of Natural and Engineering Sciences, National Institute of Advanced Studies,
Indian Institute of Science Campus, Bangalore 560012, India
e-mail: shreejata@gmail.com
A. Sinha
School of Natural and Engineering Sciences, National Institute of Advanced Studies,
Indian Institute of Science Campus, Bangalore 560012, India
Centre for Neuroscience, Indian Institute of Science, Bangalore, Karnataka, India
Nature Conservation Foundation, Mysore, Karnataka, India
e-mail: anindyaranasinha@yahoo.com;asinha@nias.iisc.ernet.in
S. Menon et al. (eds.), Interdisciplinary Perspectives on Consciousness and the Self,
DOI 10.1007/978-81-322-1587-5__9, © Springer India 2014
101
102 S. Gupta and A. Sinha
remarkably pointed out in the classic, oft neglected, paper by William James (1904).
A similar approach was recently adopted in comparative cognitive science in an
effort to dissociate a complex behaviour into its constituents and then test the
presence of these unitary building blocks across taxa (de Waal and Ferrari 2010).
We review the existing literature in human and nonhuman consciousness studies,
and aim to establish a paradigm in which particular behavioural components of
consciousness can be identified and tested across human and nonhuman species
to unravel the biological and evolutionary bases of this phenomenon. Such an
approach, we propose, will elucidate the shared features of consciousness across
taxa and broaden our understanding of the distinct levels of complexity in con-
sciousness that have arisen and manifest effectively in different species.
9.2 The Problem with Nonhuman Consciousness
9.2.1 A Definitional Problem
Scholars have identified various categories of consciousness in humans; these
include access, phenomenal, self-, subjective, transitive and narrative consciousness,
among a myriad others (Nagel 1974; Rosenthal 1986; Dennett 1991; Block 1995;
Carruthers 2000). This list, however, is not exhaustive, and multiple alternative
terms, which often overlap with one another, have been proposed to characterize
rather similar phenomena, typically involved in the manifestation of consciousness.
As problematic as it may appear, these crowds of terms, variously described by
philosophers, psychologists, cognitive scientists and neurobiologists to define and
typify consciousness, have only served to mystify and render elusive a succinct
understanding of the phenomenon. Moreover, most definitions of consciousness
appear to be specifically formulated on the basis of human attributes, stressing
on states of self-awareness and experiences of mental events that are potentially
reportable to others only through the medium of linguistic communication (Gray
2007; Kandel et al. 2008). This perhaps is a reflection of the incredible influence of
consciousness on our lives and thoughts, being the “perception of what passes in a
man’s own world” (Locke 1690).
We, however, now notice a rather pleasant change in the more recent evolutionary
approaches towards an understanding of consciousness. Novel definitions, including
words and phrases potentially more inclusive of other life forms, suggest that
consciousness is an emergent property of biological complexity, which has evolved
from “nonconscious precursors” to its extant form in humans (Seager 2007;see
also Sinha 1999a). Thus, instead of assuming consciousness to be a “mysterious”
and “unique” attribute that qualifies humans alone, it is definitely more logical to
begin a scientific enquiry into consciousness in the light of the biological continuity
that pervades extant living forms. In order to achieve this, at the very outset, we
need an all-inclusive definition that outlines the phenomenon of consciousness
9 Executive Functions as a Path to Understanding Nonhuman Consciousness. . . 103
in basic terms (see, for example, Sinha 1999b). For example, we could consider
consciousness as a state of being aware of the surrounding world (Natsoulas 1983).
This can possibly be construed to be the most fundamental form of consciousness,
which can then further incorporate different levels of complexity, manifest in the
form of more sophisticated behaviours (Posner and Rothbart 1998). Echoing the
thoughts of some contemporary philosophers, we thus propose breaking down the
concept of consciousness into its simplest possible units. Once we have a strong
base, we can then build up a concept of consciousness by adding subsequent
blocks of complexity that we encounter as we study different living forms (Searle
1998; Churchland 2002). Such a nonhuman-centric approach will, one hopes, not
only enable us to address the functional existence of consciousness, in its varied
behavioural manifestations, in different taxa but also pave the way for a better
understanding of the processes that have led to the evolution of specific cognitive
abilities in these species.
9.2.2 An Approach Problem
As briefly mentioned earlier, an important problem that our search for nonhuman
consciousness must surmount is that of the top-down approach taken by conscious-
ness studies, with virtually all investigations beginning with humans. We typically
identify various kinds of consciousness in ourselves, where consciousness perhaps
expresses itself in its most sophisticated forms. Later, we move on to establish
exactly the same expressions in other taxa, most of the times hitting a blind alley.
It will potentially be more productive to identify the processes underlying the
different behavioural manifestations of consciousness and attempt to find analogous
or homologous structures in other life forms than to expect the replica of the human
expressions in them (de Waal and Ferrari 2010). Analogous processes are those
which produce similar traits across taxa that have evolved independently, whereas
homologous processes are shared by ancestry or common descent.
Research on nonhuman and human primates, for example, has revealed homol-
ogous brain areas responsible for face recognition, a capacity that we share by
ancestry (Tsao et al. 2008;Parretal.2009). Neuroscientists could potentially follow
a similar approach, looking for neural correlates that signify processes underlying
our shared consciousness capabilities; the basic assumption in such an exercise is
not to consider the human nervous system as being unique in its conscious states.
Such a claim is obviously problematic from the perspective of our scientifically
established biological foundations. It would be far more logical and parsimonious
to assume that simple manifestations of consciousness have appeared in other life
forms and serve as evolutionary precursors for full-blown human consciousness.
Nervous systems of all taxa, therefore, possibly have the capacity to produce
conscious experience in every brain, however rudimentary they might be (Crick
and Koch 1998,2000,2003). To follow this hypothesis further, we need to begin
with brain structures that are comparatively less complex, both structurally and
104 S. Gupta and A. Sinha
functionally, in terms of their neural connections, as opposed to human brains, and
progressively factor in the complexity seen in our own neural and brain systems.
Such an approach had, in fact, been formulated from the latter part of the 18th
century and early 19th century onwards and great efforts made to understand the
neural correlates of consciousness, with an implicit assumption that all living
creatures have consciousness-like capacities (Metzinger 2000; Searle 2002; Baars
2002) and that consciousness is an emergent property of neural activities that
follow evolutionary principles (Dehaene and Naccache 2001). Some of the early
experiments to determine the neural correlates of consciousness in nonhumans were
conducted on macaques, rodents and cats and similar functionalities then tested in
humans to verify the common basis of consciousness, thus following a functional
bottom-up approach (Tong et al. 1998). These early studies were remarkable in
assuming that every nonhuman behaviour was just not a stimulus–response process
or a conditioned reflex, and such a simplistic view could never explain the mystery
of evolution of consciousness.
In this connection, one must mention the pioneering experiments conducted on
humans with visual cortex lesions, which showed that awareness is directly linked to
our visual stimuli. These experiments suggested that when an object is presented in
the “blind” visual field of blindsight patients, they have no conscious awareness of
the object (Weiskrantz 1997). The same experiments, when replicated in macaques
with segments of their visual cortex lesioned, yielded virtually identical results
(Cowey and Stoerig 1995,1997). When presented with a conditioned stimulus in
their blindsight field, the subject monkeys did not press a button to receive their
reward, as they had been trained to do, suggesting that individuals had to be visually
aware of the object to decide their next move. They were, thus, not acting on simple,
learned reflex actions to receive food as their reward.
It can, therefore, be speculated that comparative studies on consciousness and
its various aspects will ultimately reveal a conglomeration of both analogous and
homologous structures that give rise to similar behavioural manifestations of the
phenomenon across different taxa. Like any other biological feature, consciousness
too ought to follow a gradient of increasing complexity correlated with the levels
of structural advancements along the evolutionary scale. There must be certain
relationships between the brain size of an organism or the number of neuronal
connections in particular brain systems with the degree of consciousness that it
possesses. Although neuroscientists are yet to demarcate the exact number of
neurons necessary to produce any of the defined states of consciousness, capacities
like language definitely add to the complexity and nature of consciousness expressed
in humans, distinguishing it from those of nonhumans (Roth 2000). It is possibly
undeniable that, like in many other cognitive functions, humans probably represent
the pinnacle of conscious manifestations. This, however, does not take away from
the fact that there are similar functions displayed by other species. In order to
successfully conduct such comparative studies, one has to necessarily adopt a
functional bottom-up approach towards mental capacities in animals, attempts that
which promise to reveal mechanisms underlying cognitive convergence across
species over evolutionary timescales.
9 Executive Functions as a Path to Understanding Nonhuman Consciousness. . . 105
9.2.3 The Aspectual Problem
A philosophical assumption that seems to be implicit in all discussions over whether
nonhuman species are even able to recognize mental states, as a basic first step
towards the construction of more elaborate consciousness paradigms, or simply
perform behaviour analysis (as, e.g. in conditioned learning) is that the scientific
principle of parsimony is violated when mind-reading is invoked in non-verbal
nonhuman primates (Sinha 2013). Such an assumption perhaps owes its origin
to the subtle influences that biblical traditions and Cartesian philosophy seem to
have had on Western scientific ideology, which has, often implicitly, as discussed
above, valued the inherent superiority of man over all other forms of life. Although
outside the scope of this chapter, it is important to stress here that it is perhaps
now time to re-evaluate such an assumption and accept the open-minded possibility
that nonhumans may indeed possess cognitive and mentalistic capacities; rigorous
scientific methods can then be employed to investigate whether such capacities are
indeed present, as hypothesized, in these taxa.
There still continues to be a persistent problem, however, when we delve
deeper into different, more complex, aspects of consciousness. Barring the various
names that have been proposed and have multiplied over time, the problem can
be vaguely classified into the “soft” and “hard” problems of consciousness (Block
1995; Block et al. 1997). The soft problem deals primarily with issues related to
access consciousness, which includes, within its scope, discriminatory abilities,
reportability of mental states, focus of attention and control of behaviour (Long
and Kelley 2010). This problem potentially can be addressed in nonhumans as well,
provided we are able to look beyond human attributes and think in terms of relatively
simple behavioural manifestations of complex mental processes. Reportability
of mental states, for example, takes for granted an ability of language-oriented
expression. If we broaden this assumption to include any form of communicative
expression, however, we might be in a position to integrate species other than
humans alone into such a scheme. Neurobiologists have taken refuge in formulating
proxies of such reportability in clever ways. If brain imaging studies, for example,
suggest that similar brain areas are active in both humans and nonhumans during
comparable tasks that require conscious experience, at least in humans, it may be
possible to deduce that nonhuman brains have structural and functional capacities
similar to those of humans in this regard (Baars 2002). Moreover, very similar brain
responses to virtually identical stimuli presented to both human and nonhuman
brains, along with effective reportability by nonhuman species through non-lingual
means, support such findings (Logothetis 1999; Kanwisher 2001).
In contrast, the hard problem, as the name suggests, is more difficult to
deal with in nonhuman taxa, as it is even in humans. This problem concerns
phenomenal consciousness or the subjective nature of experience. Leaving aside
the question of whether we can ever understand “what is it like to be a bat”
(Nagel 1974), the explanation of qualia in humans too continues to remain a
mystery. In spite of the remarkable advantage of having that most evolved tool of
106 S. Gupta and A. Sinha
individual expression – language – we are, most of the time, at a loss to convey our
perception of the redness of a rose to our friends. An understanding of nonhuman
phenomenal consciousness, thus, appears to remain a distant dream today, as was
insightfully pointed out by von Uexküll (1934) in his classic conceptualization of
each species’ umwelt, a study that has profoundly influenced our understanding of
animal cognitive ethology.
In this essay, we mostly confine ourselves to the soft problem of consciousness
and try to tease apart the various ways we can potentially address the problem
of nonhuman access consciousness. Access consciousness, in general, can be
subdivided into two further categories: primary or core consciousness, which
provides individuals with a notion of the extant self, and extended or higher-order
consciousness, which offers an understanding of the past and the future (Tononi
et al. 1998; Damasio 2000). Scholars are generally of the opinion that primary
consciousness pervades all forms of life, whereas higher-order consciousness is a
graded phenomenon, but none are exclusively human (Damasio 2000).
9.3 Access Consciousness and Its Relation
to Executive Functions
Certain dimensions of access consciousness include behavioural manifestations
such as the use of reasoning and control of actions (Block 1995). Although this cat-
egorization was originally purely designed to explain the cognitive basis of human
behaviour, such behaviours have also been observed in a range of nonhuman species
during social interactions in specific socioecological environments. Conscious
access is critically correlated with activity in the frontoparietal networks of the brain,
apart from the perceptual networks (Sergent et al. 2005). Significantly enough,
the frontoparietal region of the brain is again associated with another group of
functions, which maps on to conscious access phenomena. These functions, which
are called executive functions, are a group of complex cognitive processes that aid in
the execution of novel tasks, flexible decision making among alternatives, working
memory, detection of errors, and the regulation of mental states and subsequently,
actions (Posner and Rothbart 1998; Stuss and Alexander 2000; Hughes 2002a). It is
also possible that the frontal lobe networks, which mostly constitute executive func-
tions, are also primarily related to emotional, motivational, social and personality
development in individuals, giving rise to a sense of self-awareness or consciousness
(Picton and Stuss 1994; Adolphs et al. 1995). Social development is clearly and
directly linked to the development of executive functioning, as is suggested by
research in child development in a two-way process. Executive functions develop
with inputs from the social environment and social skills effectively appear in
conjunction with advancement in executive functions (Luria 1973; Denkla 1996;
Hughes 2002a,b; Blakemore and Choudhury 2006). This intricate link of executive
functions and access consciousness opens up multiple doors that can lead to a
much better understanding of nonhuman consciousness: (i) there is now more direct
9 Executive Functions as a Path to Understanding Nonhuman Consciousness. . . 107
evidence of the biological and evolutionary connectivity of consciousness across
taxa in terms of analogous brain areas, (ii) consciousness is a graded concept that
potentially increases in complexity with development of neural structures across
species as well as within individuals of the same species, and (iii) consciousness
is an emergent property that can be more effectively analysed in terms of its
simpler constituent behavioural manifestations, such as the components of executive
functions.
9.4 Executive Functions in Human and Nonhuman Species
Executive functioning in humans and its direct correlates to activity in the frontal
cortex of the brain were initially discovered as by-products of investigations of
patients with brain injury, as early as in the 19th century (Harlow 1868). Systematic
explorations of frontal functions or executive functions, however, accelerated mostly
in the late 20th century, particularly with reference to processes underlying human
cognition (Miller et al. 1960;Luria1969). These investigations also focussed on war
veterans with brain injuries and the behavioural modifications that appeared in them
as an effect of such damage. This approach was eventually applied to individuals
born with psychiatric spectrum diseases such as autism. Soon enough, behavioural
variations could be predicted in people depending on the area of the brain damaged
and research in this field gained momentum in order to evaluate the functional
importance of the frontal lobe (DeKosky and Scheff 1990). Tests were also designed
to assess executive functioning scales in individuals, even in those without any
apparent anatomical damage (see Royall et al. 2002). The results obtained from
these different studies, taken together, clearly suggest that executive functions form
the building blocks of self-awareness, awareness of the world, or in other words,
access consciousness, as seen in humans. Neurobiological investigations continue
even today to identify the different functional sections of the frontal lobe and
to distinguish the separate function of each of these parts (Royall et al. 2002).
What is becoming increasingly evident, nevertheless, is the intricate nature of the
processes as well as their interactions and correlations that underlie our higher
cognitive abilities, including the different manifestations of conscious phenomena.
We are, nonetheless, still far from pinpointing a single particular neural correlate for
consciousness, although it has been controversially debated whether it is just a mere
matter of time before this is achieved.
Research on executive functions has eventually began to examine other nonhu-
man species. In fact, our understanding of the structure-function relationships within
the prefrontal cortex stems virtually exclusively from animal model systems such as
rodents and monkeys (Chudasama 2011). The discovery of anatomical homologies
between the frontal cortex of humans and those of other species has increasingly
encouraged comparative research to identify similarities and dissimilarities in the
executive functions of these different species. This has not only opened up the
possibility of study designs that involve more invasive approaches, unsuitable for
108 S. Gupta and A. Sinha
human subjects, but also allowed for a better evolutionary understanding of the
neurobiological processes involved. Experiments on rodents, for example, have
revealed functions of specific regions of the brain, including memory, attention
and behavioural flexibility, that are all remarkably similar, both structurally and
functionally, to those in humans (Kesner and Churchwell 2011).
Neural correlates and mechanisms aside, various expressions of social behaviour
in nonhuman species reflect the involvement of underlying executive functions in
their daily life. Decision making, for example, is one of the core expressions of
executive functioning, wherein a combination of processes such as discrimination
between options, appropriate reasoning based on past experience and regulation of
one’s own actions are in constant dynamic equilibrium. Various species, ranging
from honeybees to chimpanzees, make decisions on a regular basis, an indication of
the underlying frontal functions at play (Conradt and Roper 2005). To complement
these observations, the neural mechanisms underlying decision making in primates
have been traced back to neural networks primarily situated in the frontal cortex
and basal ganglia (Seed et al. 2011). Other social interactions that involve decision
making on the basis of prior knowledge of the interacting individuals, regulation of
behaviours on the basis of one’s own position and those of others in the dominance
hierarchy, and solutions to novel problems using flexible reasoning have been
reported quite frequently across taxa, including fish, birds, cetaceans and primates
(see, e.g. Sinha, Chap. 8, this volume). It is, thus, evident that neural mechanisms
in brain areas that correlate to those involved in human consciousness occur across
species and are amply manifested in their myriad behavioural interactions. Contrary
to the widely held view that human consciousness is unique, therefore, it may be
possible to argue that behavioural expressions, which reflect conscious experience,
vary considerably across species, perhaps reaching their peak in humans and that
these differences fine-tuned by evolution to different extents, are perhaps more of
degree than of kind. Such a hypothesis, however, imperatively awaits verification,
an exercise that is likely to be of crucial importance not only for cognitive ethology
in the coming years but perhaps even more significantly, for future negotiations in
human-animal relationships.
One of the most fundamental insights that we obtain during this entire exercise
of trying to understand access consciousness through its underlying neural mech-
anisms, such as executive functions, is that the concept of “core consciousness”
and “extended consciousness” as two distinct phenomena, proposed by Damasio
(2000), gradually disappears. It can now be clearly hypothesized that extended
consciousness is only possible if one possesses core consciousness and that the
development of core consciousness, which serves to develop ideas about one’s own
position in the greater world, goes hand in hand with the development of extended
consciousness. An understanding of past experiences gives way to the decisions
made in the present and in the future and, in this way, generates further knowledge
about oneself and its dynamic relationships with the surrounding world.
Let us examine an example from the animal world in some detail. When we
observe scrub jays caching seeds and returning to the same sites to retrieve them
during food shortage, we have clear observational evidence of episodic memory
9 Executive Functions as a Path to Understanding Nonhuman Consciousness. . . 109
in action, thus establishing the presence of extended consciousness in this avian
species (Clayton and Dickinson 1998). The jays can also, remarkably, distinguish
between the nature of the different food items cached, remember the duration after
which a particular kind of food perishes, and retrieve them accordingly (Clayton
et al. 2000,2001,2003). For example, when a scrub jay caches a certain kind of
larva, she seems to know that the larvae will only be edible for 4 days and she
visits this food cache within this period of time. When she has cached peanuts,
however, she revisits them relatively much later, as peanuts remains edible for longer
durations of time than do the larvae. It is illuminating to note that this capability may
indeed be widespread across the animal kingdom; episodic memory, very similar to
that of the jays and long believed to be the sole reserve of humans, has been reported
in primates (Wagenaar 1986; Menzel 1999; Schwartz et al. 2002) as also the neural
mechanisms underlying the retrieval of such memory in both human (Burianova
et al. 2010) and nonhuman primates (Hasegawa 2000).
A question that remains open in this connection is whether animals can traverse
in time while referring to episodic memories, as humans can, an ability that
once again comes under the purview of phenomenal consciousness. Although
there have been quite a few studies that have documented planning for the future
through naturalistic observations in both birds (spontaneous meta-tool use by
New Caledonian crows, Taylor et al. 2007, 2010a,b) and primates (cooperative
hunting by wild chimpanzees, Boesch 2002; deceptive stone-throwing by a zoo
chimpanzee, Osvath and Karvonen 2012), these have often been considered to
constitute circumstantial evidence alone. Experimental attempts to examine, under
controlled conditions, whether nonhumans have access to their own memories and
whether they are aware of their own awareness of events or objects around them are,
however, rare.
In an elegant memory-task experiment conducted on two rhesus macaques, the
subjects were asked to press a button if they recognized previously experienced
visual patterns (Hampton 2001). The macaques had to press one button to agree
to take the test and were subsequently shown four patterns from which they had
to choose the familiar one. Each correct choice was followed by a reward. The
experiment thus incorporated two levels of knowledge reporting by the monkeys.
In the first step, the subjects reported the absence or presence of a specific memory,
while in the next, they provided evidence of having actually recognized the pattern.
What is significant is that, after a certain time period, the monkeys did not agree
to continue the choice experiment at the first step itself, in spite of the presence
of a preferred food, thus self-reporting the absence of a memory trace. Macaques,
therefore, appear to be capable of accessing their own memory and proceed further
in a set task, depending on the status of their own knowledge (Hampton 2001).
It is perhaps time that more sophisticated experiments are designed to establish
unambiguously that nonhumans also possess phenomenal consciousness and are
capable of recollecting their own memories, as do humans, but also explore the
differences in this capacity among these species. Although one must recognize
the difficulty of recognizing true phenomenal consciousness in non-verbal species,
it may be more problematic to completely deny its presence, even if limited
110 S. Gupta and A. Sinha
in its scope, in nonhuman beings. One of the raging questions in this field is
whether phenomenal consciousness is indeed a product of access consciousness,
but notwithstanding this debate, we must keep an open mind as to the occurrence
of subjective experience, in all its nuances, in animals. The need of the day is really
the right tools to tap into them (Block 1995).
9.5 The Missing Link in Animal Consciousness
Let us now, for a moment, concentrate on access consciousness and leave aside the
ambiguous reality of phenomenal consciousness. We have a fairly clear understand-
ing of different aspects of access consciousness in humans. We have also been able
to pin down the neural correlates, such as executive functions, of phenomena related
to access consciousness. Executive functions can, thus, be considered good proxies
for access consciousness, in order to study it better, in humans. Scholars are now
comfortable relating the two terms and attributing conscious access to the frontal
cortex of the human brain (Sergent et al. 2005). In due course of these scientific
enquiries, research on frontal lobe functions has gradually expanded to nonhuman
species. Interestingly, the findings suggest human-like functions in comparable
brain areas of nonhumans, giving rise to very similar behavioural manifestations.
The fundamental proof of the presence of executive functions in nonhumans, in
their various behavioural expressions, is the prominent flexibility that these species
display across a wide range of socioecological interactions. The ability to choose
between options and form a decision on the basis of those available testifies to the
fact that nonhuman individuals are aware of the various options that are accessible to
them in the first place. Flexible innovative behavioural solutions are now common
across widely differing taxa. Tool making, for example, requires insight into the
problem, creating a mental map of the possible solutions, abstracting a particular
tool to solve the problem at hand appropriately – often by using unrelated objects –
and executing the task successfully; all these essential steps in the process require
all the attributes of executive functions, as discussed above. Tool making has now
been reported from fish, birds, elephants, macaques and apes at various levels of
complexity, both in the wild as well as in captivity (Hinde and Fisher 1951; Goodall
1964; Sinha 1997;Hartetal.2001; Matsuzawa 2001; Tonooka 2001; Chapell and
Kacelnik 2002; Laland and van Bergen 2003). In primate communication, to cite
another example, there are reports of innovative use of gestures and calls as well as
the integration of pre-existing forms to produce new sequences of communicative
signals to achieve a novel task (Cartmill and Byrne 2007; Crockford et al. 2004;
Laidre 2008; Ouattara et al. 2009).
From a variety of behavioural manifestations, many strikingly innovative, to
their underlying neural correlates, nonhuman primates, in particular, appear to
display executive functional processes in different situations, thus narrowing the gap
between our and their cognitive abilities. Theoretically then, we are now confident
of drawing parallels between executive functions and consciousness in humans and
extending this relationship to nonhuman species to which we are evolutionarily
9 Executive Functions as a Path to Understanding Nonhuman Consciousness. . . 111
linked. In reality, however, even the description of consciousness-related mecha-
nisms in nonhuman taxa does not necessarily evoke the same conclusions as it does
for humans. This is possibly, as pointed out above, a legacy of the dubious Morgan’s
cannon that proposes simplified explanations to all animal behaviour instead
of invoking higher-order capacities such as the mind or mental states (Morgan
1903). We seem to be “scientifically” destined to think about complex animal
behaviours only in terms of associative learning or other “simpler” mechanisms
instead of evoking more cognitive and occasionally mentalistic categories such as
consciousness; this is, of course, never a problem in the case of humans. Animals,
therefore, continue to be mere Cartesian automata as compared to the “uniquely”
endowed humans. Is it not time to rethink and understand afresh, both sensibly and
scientifically?
9.6 Conclusion
Studies on nonhuman consciousness have always been hindered by certain con-
straints, a major one of them being the lack of a non-anthropocentric definition of
the phenomenon. This issue, however, is intricately related to the usual top-down
approach adopted in such studies. It is crucial for us to realize that consciousness
is an emergent biological phenomenon, and as with all other comparative studies in
biology, we must begin to understand this phenomenon as it manifests in relatively
simpler organisms and work towards more complex forms, in order to unravel
its evolutionary history over relevant timescales. A second important hurdle at
this point is that it may be methodologically extremely difficult to establish the
occurrence of certain forms of consciousness, as, for example, phenomenal con-
sciousness, in nonhuman species. Insightful empirical and observational approaches
may need to be developed, if at all possible, to discover whether non-verbal species
have access to their mental states or can introspect; but if these fail, let us at least
consider the definite possibility that these individuals do have internal worlds, which
provide meaning to their lives, just as ours do for us.
Current advancements in empirical science have considerably broadened the
horizons of our understanding of higher mental phenomena. With major revolutions
in comparative psychology and cognition during the latter part of the 20th century,
we have become more accepting of the fact that processes observed in humans
can potentially be extended to other species in more contexts than one and vice
versa. Specific neurological and physiological correlates of consciousness, which
have been argued to represent conscious experience and which have now been
scientifically established to be similar across humans and nonhumans, should
be analysed even more carefully. Although it is true that causal connections
cannot be concluded easily in such complex systems, the behavioural attributes of
consciousness that are correlated to these underlying processes in humans must be
considered possible in nonhuman species with similar underlying processes as well,
subject, of course, to further rigorous validation. Emotional behaviour, for example,
has been proven to have homologous or analogous brain areas in all species, thus
112 S. Gupta and A. Sinha
strengthening Damasio’s notion of emotionality and consciousness being actively
functionally connected (Damasio 1999).
In this connection, it is heartening to note the recent declaration by a group
of cognitive scientists, psychologists and philosophers that every life form should
be assumed to possess consciousness at simplest levels, given the similarities in
behaviour and their neural correlates among humans and nonhumans (Low et al.
2012). This declaration reiterates, rather strongly, that the inability of nonhumans
to communicate through verbal language (which is also true for certain humans)
should not be held against them to insist that they are nonconscious beings. It points
out that mammalian and avian brain circuitries appear to be far more homologous
than previously discovered or suggested; it is also true that there is now increasing
interest to examine similar brain and behavioural networks in other so-called
“lower” species. The Declaration emphatically concludes that “non-human animals
have the neuroanatomical, neurochemical, and neurophysiological substrates of
conscious states along with the capacity to exhibit intentional behaviours”.
It has been believed that the mind and its different states are emergent properties
of various processes in the brain and that their existence can be inferentially
retrieved from the behaviour of humans and of other species (Hebb 1958). What
we would like to fundamentally argue here is that it is perhaps time that we look
beyond the singularity that the phenomenon of consciousness has traditionally
been considered to represent. We urgently need more bottom-up approaches of
empirically identifying the building blocks of conscious phenomena, and we
suggest executive functions to be excellent candidates in this regard. A close
examination of the processes underlying these and other functions, which have been
implicated in the generation of conscious phenomena, as well as their structural and
functional interactions in different taxa perhaps holds the greatest potential of ever
understanding what consciousness truly is and how it evolved gradually over time
to reach that pinnacle represented by our own conscious states and activities. Let us
actively and finally return consciousness to nature.
Acknowledgements Shreejata Gupta would like to thank the National Institute of Advanced
Studies, Bangalore, for a doctoral fellowship, while Anindya Sinha acknowledges a research
grant on Generativity in Cognitive Networks from the Cognitive Science Research Initiative of
the Department of Science and Technology of the Government of India. Both of us would like to
sincerely express our gratitude to Shobini L. Rao for the original idea that inspired this work as
well as for her erudition and infectious enthusiasm.
References
Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. R. (1995). Fear and the human amygdale.
Journal of Neuroscience, 15, 5879–5891.
Baars, R. J. (2002). The conscious access hypothesis: Origins and recent evidence. Trends in
Cognitive Sciences, 6, 47–52.
9 Executive Functions as a Path to Understanding Nonhuman Consciousness. . . 113
Blakemore, S., & Choudhury, S. (2006). Development of the adolescent brain: Implications for
executive function and social cognition. Journal of Child Psychology and Psychiatry, 47,
296–312.
Block, N. (1995). On a confusion about a function of consciousness. Behavioral and Brain
Sciences, 18, 227–247.
Block, N., Flanagan, O., & Guzeldere, G. (1997). The nature of consciousness: Philosophical
debates. Cambridge, MA: MIT Press.
Boesch, C. (2002). Cooperative hunting roles among Tai chimpanzees. Human Nature, 13, 27–46.
Burianova, H., McIntosh, A. R., & Grady, C. L. (2010). A common functional brain network for
autobiographical, episodic, and semantic memory retrieval. NeuroImage, 49, 865–874.
Carruthers, P. (2000). Phenomenal consciousness: A naturalistic theory. Cambridge: Cambridge
University Press.
Cartmill, E. A., & Byrne, R. W. (2007). Orangutans modify their gestural signalling according to
their audience’s comprehension. Current Biology, 17, 1345–1348.
Chapell, J. A., & Kacelnik, A. (2002). Tool selectivity in a non-primate, the New Caledonian crow
(Corvus moneduloides). Animal Cognition, 5, 71–78.
Chudasama, Y. (2011). Animal models of prefrontal–executive function. Behavioural Neuro-
science, 125, 327–343.
Churchland, P. M. (2002). Brain-wise. Cambridge, MA: MIT Press.
Clayton, N. S., & Dickinson, A. (1998). Episodic-like memory during cache recovery by scrub
jays. Nature, 395, 272–274.
Clayton, N. S., Griffiths, D. P., & Dickinson, A. (2000). Declarative and episodic-like memory in
animals: Personal musings of a scrub jay. In C. Heyes & L. Huber (Eds.), The evolution of
cognition (pp. 273–288). Cambridge, MA: MIT Press.
Clayton, N. S., Yu, K. S., & Dickinson, A. (2001). Scrub jays (Aphelocoma coerulescens)form
integrated memories of the multiple features of caching episodes. Journal of Experimental
Psychology. Animal Behavior Processes, 27, 17–29.
Clayton, N. S., Yu, K. S., & Dickinson, A. (2003). Interacting cache memories: Evidence for
flexible memory use by western scrub-jays (Aphelocoma californica). Journal of Experimental
Psychology. Animal Behavior Processes, 29, 14–22.
Conradt, L., & Roper, T. J. (2005). Consensus decision making in animals. Trends in Ecology and
Evolution, 20, 449–456.
Cowey, A., & Stoerig, P. (1995). Blindsight in monkeys. Nature, 373, 247–249.
Cowey, A., & Stoerig, P. (1997). Visual detection in monkeys with blindsight. Neuropsychologia,
35, 929–939.
Crick, F., & Koch, C. (1998). Consciousness and neuroscience. Cerebral Cortex, 8, 97–107.
Crick, F., & Koch, C. (2000). The unconscious homunculus. In T. Metzinger (Ed.), Neural
correlates of consciousness: Empirical and conceptual questions (pp. 103–110). Cambridge,
MA: MIT Press.
Crick, F., & Koch, C. (2003). A framework for consciousness. Nature Neuroscience, 6, 119–126.
Crockford, C., Herbinger, I., Vigilant, L., & Boesch, C. (2004). Wild chimpanzees produce group-
specific calls: A case for vocal learning? Ethology, 110, 221–243.
Damasio, A. R. (Ed.). (1999). The feeling of what happens: Body and emotion in the making of
consciousness. New York: Harcourt Brace and Company.
Damasio, A. R. (2000). A neurobiology for consciousness. In T. Metzinger (Ed.), Neural correlates
of consciousness: Empirical and conceptual questions (pp. 111–120). Cambridge, MA: MIT
Press.
de Waal, F. B. M., & Ferrari, P. F. (2010). Towards a bottom-up perspective on animal and human
cognition. Trends in Cognitive Sciences, 14, 201–207.
Dehaene, S., & Naccache, L. (2001). Towards a cognitive neuroscience of consciousness: Basic
evidence and a workspace framework. Cognition, 79, 1–37.
DeKosky, S. T., & Scheff, S. W. (1990). Synapse loss in frontal cortex biopsies in Alzheimer’s
disease: Correlation with cognitive severity. Annals of Neurology, 27, 457–464.
114 S. Gupta and A. Sinha
Denkla, M. B. (1996). Research on executive function in a neurodevelopmental context: Applica-
tion of clinical measures. Developmental Neuropsychology, 12, 5–15.
Dennett, D. (1991). Consciousness explained. London: Penguin Books.
Goodall, J. (1964). Tool-using and aimed throwing in a community of free-living chimpanzees.
Nature, 201, 1264–1266.
Gray, P. (2007). Psychology. New York: Worth Publications.
Hampton, R. R. (2001). Rhesus monkeys know when they remember. Proceedings of the National
Academy of Sciences of the United States of America, 98(9), 5359–5362.
Harlow, J. M. (1868). Recovery from the passage of an iron bar through the head. Publications of
the Massachusetts Medical Society, 2, 327–347.
Hart, B. L., Hart, L. A., McCoy, M., & Sarath, C. R. (2001). Cognitive behaviour in Asian
elephants: Use and modification of branches for fly switching. Animal Behaviour, 62, 839–847.
Hasegawa, I. (2000). Neural mechanisms of memory retrieval: Role of the prefrontal cortex.
Reviews in the Neurosciences, 11, 113–125.
Hebb, D. O. (1958). A textbook of psychology. Philadelphia: W. B. Saunders.
Hinde, R. A., & Fisher, J. (1951). Further observations on the opening of milk bottles by birds.
British Birds, 44, 393–396.
Hughes, C. (2002a). Executive functions and development: Why the interest? Infant and Child
Development, 11, 69–71.
Hughes, C. (2002b). Executive functions and development: Emerging themes. Infant and Child
Development, 11, 201–209.
James, W. (1904). Does “consciousness” exist? Journal of Philosophy, Psychology and Scientific
Methods, 1, 477–491.
Kandel, E. R., Schwartz, J. H., & Jessell, T. M. (2008). Principles of neural science.NewYork:
McGraw-Hill.
Kanwisher, N. (2001). Neural events and perceptual awareness. Cognition, 79, 89–113.
Kesner, R. P., & Churchwell, J. C. (2011). An analysis of rat prefrontal cortex in mediating
executive function. Neurobiology, Learning and Memory, 96, 417–431.
Laidre, M. E. (2008). Do captive mandrills invent new gestures? Animal Cognition, 11, 179–187.
Laland, K. N., & van Bergen, Y. (2003). Experimental studies of innovation in guppy. In S. M.
Reader & K. N. Laland (Eds.), Animal innovation (pp. 155–174). Oxford: Oxford University
Press.
Locke, J. (1690). An essay concerning human understanding. London: T. Basset.
Logothetis, N. K. (1999). Vision: A window on consciousness. Scientific American, 281, 69–75.
Long, L. N., & Kelley, T. D. (2010). Review of consciousness and the possibility of conscious
robots. Journal of Aerospace Computing, Information, and Communication, 7, 68–84.
Low, P., Edelman, D., & Koch, C. (2012). The Cambridge declaration on consciousness.
Conference paper presented at the Francis Crick Memorial Conference on Consciousness in
Human and non-Human Animals on July 7, 2010 in the Churchill College, University of
Cambridge.
Luria, A. R. (1969). Frontal lobe syndromes. In P. J. Vinken & G. W. Bruyn (Eds.), Handbook of
clinical neurology (Vol. 2, pp. 725–757). Amsterdam: North-Holland.
Luria, A. R. (1973). The working brain: An introduction to neuropsychology.NewYork:Basic
Books.
Matsuzawa, T. (Ed.). (2001). Primate origins of human cognition and behavior.NewYork:
Springer.
Menzel, C. R. (1999). Unprompted recall and reporting of hidden objects by a chimpanzee (Pan
troglodytes) after extended delays. Journal of Comparative Psychology, 113, 426–434.
Metzinger, T. (Ed.). (2000). Neural correlates of consciousness: Empirical and conceptual
questions. Cambridge, MA: MIT Press.
Miller, G. A., Galanter, E. H., & Pribram, K. H. (1960). Plans and the structure of behavior.New
York: Holt, Rinehart and Winston.
Morgan, C. L. (1903). An introduction to comparative psychology (2nd ed.). London: W. Scott.
Nagel, T. (1974). What is it like to be a bat? Philosophical Review, 83, 435–450.
9 Executive Functions as a Path to Understanding Nonhuman Consciousness. . . 115
Natsoulas, T. (1983). What are the objects of perceptual consciousness? American Journal of
Psychology, 96, 435–467.
Osvath, M., & Karvonen, E. (2012). Spontaneous innovation for future deception in a male
chimpanzee. PLoS ONE, 7, e36782.
Ouattara, K., Lemasson, A., & Zuberbühler, K. (2009). Campbell’s monkeys use affixation to alter
call meaning. PLoS ONE, 4, e7808.
Parr, L. A., Heckt, E., Barks, S. K., Preuss, T. M., & Votaw, J. R. (2009). Face processing in the
chimpanzee brain. Current Biology, 19, 50–53.
Picton, T. W., & Stuss, D. T. (1994). Neurobiology of conscious experience. Current Opinion in
Neurobiology, 4, 256–265.
Posner, M. I., & Rothbart, M. K. (1998). Attention, self-regulation and consciousness. Philosoph-
ical Transactions of the Royal Society B, 353, 1915–1927.
Rosenthal, D. (1986). Two concepts of consciousness. Philosophical Studies, 49, 329–359.
Roth, G. (2000). The evolution and ontogeny of consciousness. In T. Metzinger (Ed.), Neural
correlates of consciousness: Empirical and conceptual questions (pp. 77–97). Cambridge, MA:
MIT Press.
Royall, D. R., Lauterbach, E. C., Cummings, J. L., Reeve, A., Rummans, T. A., Kaufer, D. I.,
LaFrance, W. C., Jr., & Coffey, C. E. (2002). Executive control function: A review of its promise
and challenges for clinical research. Journal of Neuropsychiatry and Clinical Neuroscience, 14,
377–405.
Schwartz, B. L., Colon, M. R., Sanchez, I. C., Rodriguez, I. A., & Evans, S. (2002). Single-trial
learning of “what” and “who” information in a gorilla (Gorilla gorilla gorilla): Implications
for episodic memory. Animal Cognition, 5, 85–90.
Seager, W. (2007). A brief history of the philosophical problem of consciousness. In P. D.
Zelazo, M. Moscovitch, & E. Thompson (Eds.), The Cambridge handbook of consciousness.
Cambridge: Cambridge University Press.
Searle, J. R. (1998). How to study consciousness scientifically. Brain Research Reviews, 26,
379–387.
Searle, J. R. (2002). Consciousness and language. New York: Cambridge University Press.
Seed, A., Clayton, N., Carruthers, P., Dickinson, A., Glimcher, P. W., Güntürkün, O., Hampton,
R., Kacelnik, A., Shanahan, M., Stevens, J. R., & Tebbich, S. (2011). Planning, memory and
decision making. In R. Menzel & J. Fisher (Eds.), Animal thinking: Contemporary issues in
comparative cognition (Ernst Strüngmann forum report, Vol. 8, pp. 121–147). Cambridge, MA:
MIT Press.
Sergent, C., Baillet, S., & Dehaene, S. (2005). Timing of the brain events underlying access to
consciousness during the attentional blink. Nature Neuroscience, 8, 1391–1400.
Sinha, A. (1997). Complex tool manufacture by a wild bonnet macaque Macaca radiata.Fol ia
Primatologica, 68, 23–25.
Sinha, A. (1999a). Putting the mind back into nature: The origin and evolution of consciousness. In
S. Menon, M. G. Narasimhan, A. Sinha, & B. V. Sreekantan (Eds.), Scientific and philosophical
studies on consciousness (pp. 149–158). Bangalore: National Institute of Advanced Studies.
Sinha, A. (1999b). Almost minds? The search for consciousness in nonhuman primates. In
S. Menon, M. G. Narasimhan, A. Sinha, & B. V. Sreekantan (Eds.), Scientific and philosophical
studies on consciousness (pp. 159–167). Bangalore: National Institute of Advanced Studies.
Sinha, A. (2013). Of charitable cats and chimpanzee cultures: Reflections on the science of animal
behaviour and cognitive ethology. In B. V. Sreekantan (Ed.), Foundations of sciences.New
Delhi: Centre for Studies in Civilizations.
Stuss, D. T., & Alexander, M. P. (2000). Executive functions and the frontal lobe: A conceptual
view. Psychological Research, 63, 289–298.
Taylor, A. H., Hunt, G. R., Holzhaider, J. C., & Gray, R. D. (2007). Spontaneous metatool use by
New Caledonian crows. Current Biology, 17, 1504–1507.
Taylor, A. H., Elliffe, D., Hunt, G., & Gray, R. D. (2010a). Complex cognition and behavioural
innovation in New Caledonian crows. Proceedings of the Royal Society B, 277, 2637–2643.
116 S. Gupta and A. Sinha
Taylor, A. H., Medina, F., Holzhaider, J. C., Hearne, L., Hunt, G. R., & Gray, R. D. (2010b). An
investigation into the cognition behind spontaneous string pulling in New Caledonian crows.
PLoS One, 5, e9345.
Tong, F., Nakayama, K., Vaughan, J. T., & Kanwisher, N. (1998). Binocular rivalry and visual
awareness in human extrastriate cortex. Neuron, 21, 753–759.
Tononi, G., Srinivasan, R., Russell, D. P., & Edelman, G. M. (1998). Investigating neural correlates
of conscious perception by frequency tagged neuromagnetic responses. Proceedings of the
National Academy of Sciences of the United States of America, 95, 3198–3203.
Tonooka, R. (2001). Leaf-folding behavior for drinking water by wild chimpanzees (Pan
troglodytes) at Bossou, Guinea. Animal Cognition, 4, 325–334.
Tsao, D. Y., Moeller, S., & Freiwald, W. A. (2008). Comparing face patch systems in macaques
and humans. Proceedings of the National Academy of Sciences of the United States of America,
105, 19514–19519.
von Uexküll, J. (1934). A stroll through the worlds of animals and men. In C. H. Schiller (Ed.),
Instinctive behaviour (pp. 5–80). New York: International University Press.
Wagenaar, W. A. (1986). My memory: A study of autobiographical memory over six years.
Cognitive Psychology, 18, 225–252.
Weiskrantz, L. (1997). Consciousness lost and found. Oxford: Oxford University Press.
