Afference copy as a quantitative neurophysiological model for consciousness

Aerence copy as a quantitative neurophysiologicalmodel for consciousness

Hugo Cornelis and Allan D. Coop*

Three Way Street, P. O. Box 5160, BraddonAustralian Capital Territory 2612, Australia*[email protected]

[Received 27 March 2014; Accepted 7 April 2014; Published 20 June 2014]

Consciousness is a topic of considerable human curiosity with a long history of philosophicalanalysis and debate. We consider there is nothing particularly complicated about conscious-ness when viewed as a necessary process of the vertebrate nervous system. Here, we propose aphysiological \explanatory gap" is created during each present moment by the temporalrequirements of neuronal activity. The gap extends from the time exteroceptive and propri-oceptive stimuli activate the nervous system until they emerge into consciousness. During this\moment", it is impossible for an organism to have any conscious knowledge of the ongoingevolution of its environment. In our schematic model, a mechanism of \aerence copy" isemployed to bridge the explanatory gap with consciously experienced percepts. These perceptsare fabricated from the conjunction of the cumulative memory of previous relevant experienceand the given stimuli. They are structured to provide the best possible prediction of theexpected content of subjective conscious experience likely to occur during the period of thegap. The model is based on the proposition that the neural circuitry necessary to supportconsciousness is a product of sub/preconscious reexive learning and recall processes. Based ona review of various psychological and neurophysiological ndings, we develop a frameworkwhich contextualizes the model and briey discuss further implications.

Keywords: Consciousness; explanatory gap; aerence copy; reex; inhibition; learning; mem-ory; prediction; qualia; review.

1. Introduction and Philosophical Context

Although much is currently known about the vertebrate central nervous system

(CNS), little is known about the emergence of consciousness. Guided by philosophical

considerations, we review known psychoneurophysiological data to provide a plau-

sible framework for conscious experience. This framework is developed from dem-

onstrated neural properties that are widely considered fundamental to CNS

operations, including: reex activity (Sechenov, 1863), its organization (Sherrington,

1906) and timing (Maniadakis & Trahanias, 2014); and the role of inhibitory pro-

cesses (Lee & Maguire, 2014; Schel et al., 2014), learning (Pavlov, 1927; Thorndike,

1911) and memory (Brown et al., 2007; Hebb, 1949). In doing this, we nd a possible

explanation for the origin of qualia within the CNS.

Journal of Integrative Neuroscience, Vol. 13, No. 2 (2014) 363402c Imperial College PressDOI: 10.1142/S0219635214400020

363

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Following satiation of biological imperatives such as survival and reproduction,

probably no other issues have come to stimulate human curiosity more, in one way or

another, than the descriptive, functional and explanatory mysteries surrounding the

idea of consciousness. It is an idea with which all thinking persons can engage as it is

central to the problem of how we understand the world including ourselves and our knowledge as part of the world, see Popper (1959). The challenge is to make

sucient room in our models of cosmology and the general nature of reality to permit

a consistent account of consciousness, and vice versa our notions of consciousnessmust accommodate an understanding of what it means for its content to be \reality

as a whole" (Bohm, 1980). However, over 2000 years of curiosity (Koch, 2009) seems

to have added little of substance to either discussion or knowledge.

Three considerations provide a context for the framework we develop. The rst

concerns Sherrington's (1940) contemplation of the planet, \furnace of molten rocks

and metals, now yielding thoughts and values. Magic furnace. Beside its alchemy and

transmutations the most impassioned dreams of Hermes Trismegistus and all his

fellowship dwindle to paltry nothing". The second proposes that, \problems are

solved not by giving new information, but by arranging what we have known since

long". (Wittgenstein, 1953). The third states that, \At stake are central key concepts

that directly involve fundamental convictions regarding the nature of man's inner

being, physical reality, the meaning of existence and related matters of ultimate

concern. . . . perspectives in this area profoundly shape human value systems and

societal decision-making and hence human destiny". (Sperry, 1980).

In short, (1) A remarkable structural evolution of matter has occurred, (2) we

already know much of what is needed to solve the problem of consciousness and (3)

we interpret and structure the world based on our understanding of how the brain

works. Importantly, we consider many problems of consciousness would evaporate if

it is accepted that construction of internal representations or replicas of the \outside"

world is unnecessary (Velmans, 2009). For as O'Regan (1992) and many others have

proposed it is continuously available \out there".

Depending upon the gure of speech chosen, consciousness has been identied with:

a state of being, a substance, a process, a place, an epiphenomenon, an emergent aspect

of matter, or the only true reality (Miller, 1962); and described as a fascinating but

elusive phenomenon for which it is impossible to specify what it is, what it does, or why

it evolved; with little worth reading written about it (Sutherland, 1989).

In the cognitive realm, nowhere has a dominant metaphor been more central and

susceptible to \sporadic reformulation" in terms of the technology of the day than

when theorizing about the brain (Daugman, 1993). For example, the following

metaphors, ranging from cosmological to mathematical, have all been employed:

embodied spirits and helmsmen (Arbib, 1972); hydraulics and mechanics (Vartanian,

1973, 1953; Resniko, 1988); electricity (von Helmholtz, 1850a,b; Hebb, 1949;

Hodgkin & Huxley, 1952) and optics (Pribram, 1969); networks of simple automata

and societies of mind (Dennett, 1978; Minsky, 1988); determinism of the unconscious

and automatic (Freud, 1904/1914); logical calculus of neurons (McCulloch & Pitts,

364 H. CORNELIS & A. D. COOP

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1943); the stochastic Boltzmann machine, spin-glass latices, Ising spins (Hopeld,

1982; Hinton & Sejnowski, 1986; Gutfreund et al., 1988) and chaotic dynamics and

attractors (Skarda & Freeman, 1987). Given such historical antecedents, it is

probably shortsighted to regard the current metaphors of the brain as information

processor and computer (Pylyshyn, 1986) or container of representations (Nadel &

Piattelli-Palmarini, 2003) as entirely dierent kinds of breakthrough in the history

of ideas.

Ever since publication of the classic paper by Nagel (1974), \What is it like to be a

bat?", the \intractable problem of consciousness" Churchland (1996), has been

identied as, how is it that consciousness of subjective experience is possible? This is

known as the \Hard Problem" (Chalmers, 1996), and concerns, \how and why

consciousness arises from physical processes in the brain" (Chalmers, 1997).

The \explanatory gap" is a philosophical term related to the \Hard Problem". It

refers to the lack of an explanation of how physical properties give rise to the qualia of

experience (Levine, 1983). We take a more pragmatic view of this problem than

those who consider it represents the limits of current knowledge (Churchland, 1996),

or of cognitive abilities (McGinn, 1989), or necessarily entails a metaphysical gap

(Chalmers, 1996).

Nevertheless, consciousness continues to be a prominent mystery for philosophy

and science (Chalmers, 1996). Initially, the preserve of philosophy, more recently

quantitive empirical studies have become both more accepted, and possible; with

rapid advances over the last two decades (Price & Barrell, 2012), as ongoing devel-

opment of experimental techniques and new observations drive theory and research

(Blackmore, 2001).

We are, of course, unhappy with much proposed for the \problem" of conscious-

ness, whether hard or otherwise. The fact that philosophers are forced to deny its

existence (Dennett, 1991), solve it by attribution of as yet unidentied irreducible

properties (Chalmers, 1996), or claim it is beyond the limits of human knowledge

(McGinn, 2004), seems somewhat unsatisfactory.

Our starting position is therefore similar to that of Churchland (1996); to partition

the mind-brain problem as Chalmers (1996) has done, \poses the danger of inventing

an explanatory chasm where (all that really exists is) a broad eld of ignorance". The

only conclusion from the fact that consciousness is mysterious, is that its mechanisms

are not understood. From the vantage point of ignorance, it is dicult to tell which

problems actually are harder and which will be solved rst. As Churchland (1996)

suggests, \learn the science, do the science, (then) see what happens".

The essence of the model presented here is a transguration of the philosophical

explanatory gap into a neurophysiological context. This allows the introduction

of a plausible \aerence copy" mechanism which bridges an otherwise inescapable

physiological explanatory gap. In doing so, we address the confounding observations

reported by Libet (2004, 1985), and more recently by Soon et al. (2008) and Bode

et al. (2011). The issues involved concern the timecourse of sensory stimulation and

voluntary motor acts and their emergence into consciousness.

AFFERENCE COPY AS A QUANTITATIVE NEUROPHYSIOLOGICAL MODEL 365

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In proceeding, we aim to contribute to improved clarity of understanding by

rening concepts which may not previously have been well articulated. To this end,

we aim to explain, \How it is that subjectively we seem to exist in a seamlessly

perpetual and detailed present moment".

2. Considerations Developed About Consciousness in Dierent

Temporal and Phylogenetic Domains

In this section, we introduce biological considerations which assist in framing the

model presented here. We begin by noting that Penrose & Hamero (2011) report the

recognition of three general possibilities for the origin and place of consciousness in

the universe: (1) It is a quality that has always been in the universe, (2) precursors

have always been in the universe and biology evolved a mechanism to convert con-

scious precursors to actual consciousness or (3) it is not an independent quality but

has arisen as a natural evolutionary consequence of the biological adaptation of

brains and nervous systems,

Alternatively, the three major theories of consciousness taken most seriously by

neuroscientists include the view that (Block, 2009): Consciousness (1) must be

described in terms of higher order states, (2) is a property of a global workspace or

(3) is a biological state of the brain.

Solms (1997) has proposed the totality of human consciousness consists of three

domains: (1) Primary external perceptions experienced as material reality; (2) pri-

mary internal perceptions (aect) and (3) perceptions of activated traces of previous

experiences (memory and cognition), the latter two being experienced as introspec-

tive awareness (or psychic reality).

Alternatively, Tulving (2002) has proposed three forms of consciousness:

(1) Anoetic or \unthinking", which may be aectively intense, (2) noetic or cognitive

activity linked to the physical instantiation of the objects of exteroceptive perception

and (3) autonoetic or higher neocortical functions including, abstract perceptions

and cognition, conscious (self) awareness and reection on episodic memory, pre-

dictions of the future and fantasy or hallucination.

Solms & Panksepp (2012) mapped the preceding scheme to phylogenetic evolution

of: (1) Upper brainstem and septal areas (anoetic phenomenal experience), (2) lower

subcortical ganglia and upper limbic structures of the cortical midline (noetic con-

sciousness and learning) and (3) association cortex, providing the critical substrates

for \reexive experiential blends that yield the stream of everyday awareness"

(autonoetic consciousness).

2.1. Consciousness a reduction to fragmentsIf self-awareness is taken as evidence for consciousness, then in evolutionary terms

consciousness may have rst appeared about 5 million years ago and be at least as old

as the placental divide in mammals (Wildman et al., 2007), with the foundations

of consciousness and self-consciousness possibly formed as early as the amniote


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radiation (Warren et al., 2008). The core of human consciousness is thought to have

originated in phylogenetically ancient structures activated by primitive emotions

mediating arousal, in conjunction with limited connectivity with frontalparietal

areas (Mashour & Alkire, 2013).

It has been well demonstrated that the operations of the CNS add color, sound and

a multiplicity of sensations to continual sampling of reality. This sampling is recorded

with remarkable veracity from atomic and quantum domains (Kaupp, 2010; Smith,

2002; Hecht et al., 1942). Such detail is likely captured at a resolution sucient for

the existence of physical phenomena to be demonstrated, quantied, modeled and

ultimately, understood.

The cerebral cortex is currently considered to be the primary site containing the

neural correlates of awareness (Mashour & Alkire, 2013). From a top-down perspec-

tive, evidence for this includes the desynchronized nature of the electroencephalogram,

activity in the thalamocortical systemandwidespreadbrain activity (Seth et al., 2005).

The coupling of an internally based need system with an externally directed sit-

uational awareness system is considered to provide a basis for the emergence of

consciousness and has been shown to be closely related to the mental machinery seen

in humans for generating arousal and awareness (Mashour & Alkire, 2013). The most

basic emotions and arousal states are associated with internal feedback networks that

guide an organism's behavior to the best possible outcomes. This functionality is

considered to underly essentially all behavioral choices in the vertebrate brain

(Mashour & Alkire, 2013).

One feature of experience putatively identied by philosophers is an insubstantial

component of consciousness called qualia. These have been dened as the internal

and subjective components of sense perceptions, arising from stimulation of the

senses by phenomena; they are recognizable qualitative characters of the given, which

may be repeated in dierent experiences, and are thus a sort of universal (Jackson,

1982). Qualia involve the subjective experience of the redness of red, the painfulness

of pain and so on.

At a psychological-level, Freud (1915) considered mental processes are in them-

selves unconscious and that their perception by consciousness is similar to the per-

ception of the external world by the sense-organs. Unconscious mental activity is

therefore similar to all other natural processes (Solms, 1997), with most of mental life

unconscious most of the time, only becoming conscious as sensory percepts, such as in

words and images (Gray, 2002). Jackendor (1987) considers consciousness is not a

particularly high-level process, as everyone has always wanted it to be, and that \it is

not what makes us human".

Besides subjectivity, in humans at least, conscious life has two other dominant

features: unity and intentionality. The unitary nature of consciousness refers to the

appearance of subjective brain experiences as unied, integrated and a constructed

whole (Kandel, 2000b). Intentionality refers to the typical focus of consciousness

being about objects or events (Edelman, 2003), with emotional (LeDoux, 2000) and

semantic aspects (Chalmers, 1996), being central.


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Ingvar (1985) considers conscious experience is based on three components:

memory of the past, experience of \actual events in the now-situation" and concepts

of the future or events which have not yet occurred. For him, the important question

is, \to what extent do events in the brain, related to the past, the present and

the future, take place at a conscious-(attentive) level or at a subconscious (pre- or

subattentive-level) or at both levels simultaneously".

In answering this question, Jackendor (1987) proposes that the character of the

phenomenological mind is comprised of unconscious and conscious elements but

that processing is always unconscious; in short, processes are never available to

consciousness in perception, thought, learning or action.

Many treatments of consciousness in the literature recognize, at least incipiently

(Jackendor, 1987), that consciousness is projected from mental information struc-

tures, where the stream of consciousness, made up of visual and verbal imagery, is

usually sucient to be believed to constitute thought. But Jackendor (1987) con-

siders this may not actually be the case. Rather, visual and verbal images emerge

from intermediate structures, which are in turn generated from thought by manda-

tory fast processing modules. Hence, the stream of consciousness is essentially

nothing but evidence that thought is occurring in a subconscious domain, with both

the process of thought and its contents inaccessible to awareness.

Importantly, the fact that human cognitive processes are largely nonconscious has

been periodically reported, although often ignored. von Helmholtz (1910) observed

that we are not aware of the elements used to form a judgement we make\unconscious interferences" based on prior experience. Lashley (1956) further em-

phasized, \No activity of mind is ever conscious . . .Experience clearly gives no clue as

to the means by which it is organized". We are not conscious of the details that make-

up a percept. Such details are inhibited from our conscious awareness. Instead, what

is seen depends largely on what is already known (Snyder, 1998; Snyder & Barlow,

1986; Gregory, 1970). Basically, every image is forced to t into a known percept

(Snyder et al., 2004).

This perspective on human perception is also strongly supported by reports of

detail blindness (No, 2007); e.g., change (Simons & Rensink, 2005; O'Regan, 2003),inattentional (Mack & Rock, 1998) and repetition (Kanwisher, 1987) blindness; and

the attentional blink (Chun & Potter, 1995; Raymond et al., 1992). Space precludes

further review of this extensive literature, which we consider provides compelling

support for our conjectures.

Following a comprehensive review, Velmans (1991) concludes no human infor-

mation processing is conscious in the sense that consciousness enters into or causally

inuences the process. What enters awareness follows the processing to which that

awareness relates.

Similarly, Berlin (2011) concludes that complex cognition can proceed in the

absence of consciousness, that the unconscious brain is active, purposeful and inde-

pendent and can selectively access and activate implicit goals and motives. However,


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he notes that exactly how unconscious emotions and evaluations help shape the

dynamics giving rise to conscious perception is still unknown.

Gray (2004) has postulated three aspects of consciousness: (1) It contains a model

of the relatively enduring features of the external world which is experienced as

though it is the external world, (2) features that are particularly relevant to ongoing

motor programs, or which depart from expectation, are monitored and emphasized,

(3) The control variables and set-points of the brain's nonconscious servomechanisms

are juxtaposed, combined and modied; in this way, error can be corrected.

At the core of his model is a \comparator", which compares actual stimuli with

expected stimuli a function performed by a behavioral inhibition system (Corr,2008). When there is no discrepancy, behavioral routines run uninterrupted and

stimuli are not extracted for detailed processing by higher-level cognitive processes.

When mismatch is detected between actual and expected states of the world, the

alien features of the error-triggering environment are subjected to controlled, at-

tentional, analysis and (often) emerge into conscious awareness.

Perlovsky (2013) notes, brain imaging experiments have demonstrated that vague

mental states and the entire dynamic logic process (taking approximately 500ms) are

unconscious. Only nal near-logical sensory percepts become available to con-

sciousness. Most brain operations (more than 99%) are inaccessible to subjective

consciousness, while the mind operates by \jumps" among \islands" of conscious-

logical states in an ocean of unconsciousness. In short, we are subjectively convinced

of our consciousness. Further, in a recent review, Aru & Bachmann (2014) argue that

attention and consciousness are independent from each other and phenomenal con-

sciousness can emerge without attention.

2.2. Timing of the phenomenology of consciousness

Following Donders (1868), three fundamental response latencies or reaction times

have been conrmed, \simple", \recognition" and \choice" (Baayen & Milin, 2010).

For simple reexes in humans, the shortest reaction times are those of the uncon-

scious blink reex with a mean latency of 10.8ms (Shahani, 1970); whereas, reex

latencies formuscle in response to electrical stimulation range from 3151ms (hand) to

5581ms (foot) (Tarkka, 1986). Similarly, response times of 810ms (auditory)

(Kemp, 1973), 2040ms (visual) (Marshall et al., 1943) and 155ms (touch) (Robinson,

1934), have been reported.

Although, subjectively, recognition of familiar objects and scenes appears virtually

instantaneous, this actually is not the case. For example, event related potentials in a

visual recognition task show the visual processing required to identify an animal in a

visual scene viewed for 20ms requires up to 150ms, with reaction times of 382567ms

(median 445ms, Thorpe et al., 1996).

We consider that on purely empirical grounds, these ndings argue directly

against any immediacy whatsoever for the phenomenology of consciousness. In

support of this position, in the following section (as one amongst several possible


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examples), we further briey explore vision in more detail. In particular, its temporal

properties and implications.

2.3. The problem of the rapid establishment of visual consciousness

Principled estimates of the timing of visual activity can be made. For example, any

activity requiring detail or color (e.g., driving or reading) must be located within the

foveal area by a saccade. The fovea occupies less than 1% of retinal area but over 50%

of the visual cortex (Krantz, 2012). It covers about two degrees of the visual eld or a

disc about 4 cm in diameter at arm's length. In vertebrates, the fovea may be com-

pared to the location where axons converge to form the head of the optic nerve. The

resulting hole in the photoreceptor mosaic is up to six times the foveal area, which at

35 forms a surprisingly large \blind spot", equivalent to a 610 cm diameter discat arm's length (O'Regan, 1992).

Dierent saccades (Hopp & Fuchs, 2004), exhibit remarkably stereotyped

amplitude, duration and peak velocity (Becker, 1989). Their dynamics are deter-

mined by the point of origin within the visual eld and the trajectory of movement

employed to locate a target. Typically, they last about 25190ms for movements of

560, respectively (van Beers, 2008).Reactive targeting saccades exhibit latencies of about 180ms (Smit et al., 1987),

but may be as fast as 100135ms (Fischer & Ramsperger, 1984; Fischer et al., 1993),

whereas, memory-guided saccades may take well over 200ms (Hopp & Fuchs, 2004).

The duration of the minimum ocular pause time in the absence of stimulus pro-

cessing is about 200ms, with processing requiring an additional minimum 50100ms

(Salthouse & Ellis, 1980). Although, for example, when reading, information may be

extracted from foveal input within about 50ms (Rayner et al., 1981), with ocular

pauses of 100200ms duration (van Diepen et al., 1995; Harris et al., 1988). Im-

portantly, saccade optimization probably occurs during development rather than

being innate (van Beers, 2008), as the dynamics of equivalent saccades vary across

subjects (Boghen et al., 1974; Schmidt et al., 1979).

The number of foveal xations (Nf ) required to cover the area of the binocular

visual eld can be estimated from the number of square degrees (Guthrie, 1947), in

the visual eld (Av) and fovea (Af ):

Nf AvAf

2 200 135

2 2 2

17; 1892:5465

6; 750:

If the optimal duration of a two-degree saccade is assumed to be 30ms (van Beers,

2008) and the minimal ocular pause 100ms (well below the 250ms required for visual

processing), the time required to scan the entire visual eld at foveal resolution with

7.5 xations s1 is about 15min. A more physiologically realistic rate of three xa-tions s1 would require up to 37.5min.

Given these gures, it is not surprising that an infant takes several months to

develop, or more preciselylearn, accurate hand-eye coordination. However, what is


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surprising is adults subjectively experience a very rapidly established high resolu-

tion global visual acuity in familiar environments. The question is, given that for

any one viewpoint this should take almost 40min to establish, how is it so rapidly

generated?

A partial answer is provided by Hebb (1949) who suggests, \during the continu-

ous, intensive and prolonged visual training of infancy and childhood, we learn to

recognize the direction of line and the distance between points, separately for each

grossly separate part of the visual eld". Further, \[I]t takes months for the rst

direct apprehension of a gure such as a plain, well-marked triangle to be established.

The normal human infant, apparently, reaches this stage quite early in life; but his

further training continues every moment that his eyes are open, and must extend his

capacity for prompt recognition of patterns falling outside the macula. . . . The sig-

nicant fact is that characteristic normal generalization only shows up after a pro-

longed and arduous training process."

There is every reason to expect that similar extended training occurs with other

senses. In summary, it would seem rapid establishment of consciously experienced

perception may actually be enabled by prior learning; following sensory activation,

percepts are evoked as required from the memory system.

2.4. The subjective antedating of perception

Two main types of organization of specic aerent systems have been reported for

vertebrates (Voronin et al., 1968): (1) Individual sensory modalities in sh partition

to dierent brain structures, whereas, (2) in mammals, all sensory modalities are

collected in the forebrain. Those of amphibians and reptiles lie between these two

bounds. Regardless of how basic human sensory modalities are classied, the dierent

perceptual qualities they generate are the constituent elements of the envelope of

consciousness and nothing else exists (Solms, 1997).

A basic problem related to the conscious perception of stimuli and initiation of

voluntary activity has been identied. Many studies conrm that, close to sensory

threshold, a delay of up to about 500ms occurs before cerebral activities initiated by

stimulus detection systems achieve the duration and intensity of stimulation or

\neuronal adequacy" necessary to successfully elicit conscious awareness of the

stimulus (Libet et al., 1964). (Although, stronger stimuli may reduce this delay to as

little as 100ms.) The problem is that following neuronal adequacy, the subjective

timing of the experience appears to occur without the actual delay required for

neuronal adequacy to elicit conscious experience of the stimulus.

One inference from such a result is that the experience of a skin-induced sensation

is elicited at a cerebral-level with a much shorter delay than for cortically-induced

sensation, an explanation discounted by Libet (1981).

As a solution to this problem, Libet (2004) has proposed that following neuronal

adequacy, subjective timing of the experience is automatically referred backwards to

the moment when primary sensory cortex received the stimulus (2025ms after


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peripheral stimulation). The experience is thus \antedated" and subjectively appears

to occur without the substantial delay required for conscious experience of the

stimulus.

Below, we provide a less paradoxical explanation. It forms the basis of the

\aerence copy" model.

2.5. Emotion

For completeness, we now make a few comments about the role of emotion in neural

function. (For more details, see for example, LeDoux (1996)). In a review, Vuilleu-

mier & Huang (2009) report that interactions between brain systems involved in

emotion and attention may contribute to regulating behavior and awareness by

enhancing relevant sensory information. Emotional stimuli may also evoke uncon-

scious reexive and involuntary processing under many conditions. Further, invol-

untary monitoring of emotional stimuli and reexive boosting of perceptual processes

may reect some \default" settings or intrinsic preparedness within neural pathways.

They can also be adaptively shaped by various regulatory mechanisms that them-

selves operate potentially with or without conscious control. Finally, we note Solms

(1997) proposes that aect must be considered a sensory and perceptual modality.

3. Biological Framework for a Model of Consciousness

Based on the foregoing, and as outlined in more detail below; we present a model

where unconscious precursors of the conscious experience of each given moment are

molded within the memory system by integration with aerent stimuli (including

emotional aects experienced as qualia).

Our claim is that through the physiological mechanisms supporting this model,

the repetitive nature of a purely reexive existence is transcended, content created

and subjective experience expanded. Through these underlying mechanisms, the

cumulative procession of known prior events and activities inform current experience

and, via a surprisingly counter-intuitive mechanism, lay the basis for future behavior.

Each successive moment is formed from, and experienced through, the cumulative

record or memory of all relevant previous moments. In the deepest sense, each

present moment is the last remaining moment; experienced not in its encapsulation of

the past, but as an experience bounded prediction of the future.

From this perspective, we consider there is sucient empirical data to formulate

several broad conjectures from which a framework for consciousness might be

developed:

(1) With the exception of innate reexes (Zafeiriou, 2004), non-conscious activity in

the CNS is generated, organized and controlled through elaboration of reex

circuits assembled by associative learning.

(2) Inhibitory processes are the preeminent mechanism whereby the CNS controls

neural activity.


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(3) All CNS functions, from meaningful integration of sensory stimuli to con-

sciousness and generation of motor plans, arise from ongoing (prenatally initi-

ated) renement of learning.

(4) Memory is a repository for learning and throughout life it is continually formed,

and modulated, by accumulated moment-to-moment sampling of all available

sensory modalities.

(5) The physics of CNS function requires, and evolutionary pressures drive increased

capacity for anticipatory prediction.

We now briey explore evidence supporting these conjectures.

3.1. From spinal cord reexes to reexive behavior

The reexive nature of nervous systems is an evolutionary requirement imposed by

the need for control of reliable response in ever-changing and dynamic environments.

Thus, Sechenov (1863) was convinced that, \as far as the presence in man of three

separate mechanisms directing the phenomena of conscious and unconscious life is

concerned (viz. the mechanisms of the pure reex, and those of reex inhibition and

augmentation). Let anyone who thinks this hypothesis is doubtful, even poorly

demonstrated, or simply unacceptable, controvert it . . .If anyone nds a better

explanation, I shall be the rst to welcome it".

Since the early 19th century, it has been recognized that \just as the spinal reexes

[bear] a `genetic' anity to the irritability of the simplest animals and of plants, so

the operation of the highest nervous centers in humans [retain] the fundamental

reex character of the lower" (Clarke & Jacyna, 1987). For example, Laycock (1845)

concluded that, \the ganglia within the cranium being a continuation of the spinal

cord, must necessarily be regulated as to their reaction on external agencies by laws

identical with those governing the functions of the spinal ganglia and their analogues

in the lower animals".

Sechenov (1863) was the rst to propose that all aspects of cognition in humans

are based on behavioral reexes or more generally that reex circuits provide the

basis of all nervous function.

During the 19th century, the reex concept became basic for attempts to explain

the physiological functioning of the nervous system. By the end of the century the

tendency was to include increasing parts of animal behavior under reexive move-

ments; that is, movements elicited through stimulation originating from an organ-

ism's external or internal milieu.

Early in the 20th century the reex arc was established as the functional unit in

CNS integration (Sherrington, 1906). Magnus (1924) demonstrated the reex nature

of all the elementary motor activities, and it was believed stereotyped movements,

such as those involved in walking, swimming and other locomotion, could be ana-

lyzed and described in terms of reexes. Sequential patterns of eector activity were

explained as arising from coordinated patterns of exteroreceptive and proprioceptive


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excitation of the CNS. Richet (1925) introduced \the conception of the psychic reex,

in which the response following on a given stimulus is supposed to be determined by

the association of this stimulus with the traces left in the hemispheres by past

stimuli". In summary, the reex concept was used to explain the integrative functions

of the brain previously considered to result from \psychic activities" (Jrgensen,1974).

Subsequently, motor-related activity in the CNS was shown to not necessarily

reect corresponding patterns of peripheral sensory activity. Thus, it was assumed

animal locomotion and other types of movements are determined by central pattern

generators, where the role of peripheral stimulation and sensory feedback is to

activate and modulate these generators (Bullock, 1961).

More recent interpretation suggests pattern generators may be intrinsic spinal

processors comprised of hybrid feedforward/feedback systems which optimally

compensate for both disturbances and sensor noise and can adapt central input to

this optimized peripheral input (Kuo, 2002). This is not inconsistent with pattern

generators being viewed as examples of sophisticated reex circuits.

The denition of a reex has been quite variable, ranging from the restrictive,

\stimulus-evoked response that usually involves a single muscle or a limited group of

muscles" (LeDoux et al., 2009), to the more general, \all neural processes (or neural

responses) and following eector responses evoked by any currently acting stimulus",

where a stimulus is a physical event (or a change in physical energy) which elicits the

activity of sensory receptors or higher-levels of the aerent nervous system ( Zernicki,

1968). In short, a reex is an automatic or involuntary and near instantaneous

response to a stimulus. Importantly, it is possible to conclude a reex circuit may be

activated by any sucient stimulus.

As McCulloch (1947) has clearly stated, modes of functional organization of the

cerebral cortex are reexive: \To that great extent to which its aerents inform it of

the peripheral consequences of the action of its own eerent, any system is part of the

path of a reex".

Complex or chain reexes located in the CNS have been demonstrated to consist of

a number of unitary processes, for which feedback control is essential ( Zernicki,

1968). Further, Slonim (1968), notes that complex, obligate stereotypic behavior

generated on the base of natural conditioned reexes in contrast to articial orfacultative trainingare components of specic adaptive behaviors required under

dierent ecological conditions of existence.

Both simpler innate and more complex behavior comprising chains of individual

motor acts can generate and repeat themselves stereotypically and independently of

the conditions of postnatal development. Thus, between the \instinct" and the

\unconditional reex" there is a chain of stages dependent on either reex or the

automatic nature of nervous system activation (Slonim, 1968).

It is well-known in humans that, introspectively, some stimuli produce psychic

responses which may be assumed present in higher animals (Doty, 1967; Thorpe,

1966; Beritov, 1965). It has further been assumed that cerebral responses are


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manifestations of denite unitary central processes or neuropsychic processes, of

which there are several kinds: eectively indierent or gnostic processes, or un-

pleasant or pleasant processes that are negative or positive emotions, respectively.

Psychic responses may additionally be divided into perceptions and images.

Signicantly, Konorski (1967) hypothesized that both perception and image are

manifestations of excitation of the same neurons, with the dierent psychic responses

(perception vs. image) due to dierent ways of exciting these neurons; from the

periphery and by association, respectively. There is a good reason to believe neu-

ropsychic processes are located in the cerebrum, gnostic processes mainly in asso-

ciative cortex, and negative and positive emotional processes in dierent places of the

limbic system and hypothalamus ( Zernicki, 1968; Olds, 1956). Importantly, this

seems to map well with the schemes of Tulving (2002) and Solms & Panksepp (2012)

mentioned above.

More recently, LeDoux et al. (2009) proposed that many behaviors fall into one of

four categories: reex, reaction, action and habit; where habit formation (the most

complex) and much of learning are dependent on conditioned reexes. For example,

the brain of a student typist must coordinate sensory impulses from both eye and

muscle to direct their ngers to particular keys. After sucient repetitions, the

ngers automatically nd and strike the proper keys even when the eyes are shut.

The student has \learned" to type; that is, typing has become a constellation of

conditioned reexes (Lagasse, 2000).

The simplest neuronal circuits are the monosynaptic reex arcs composed of one

sensory neuron and one motoneuron, for example, the circuits subserving the patellar

or achilles reex. Sherrington (1906) considered the whole nervous system to be based

on this type of circuit, \even those of the cortex of the cerebrum itself". However, all

but the simplest reex circuits are polysynaptic, where one or more interneurons are

interposed between the aerent (sensory) and eerent (motor) neurons of the

monosynaptic circuit.

Once again, Sechenov (1863) has asked, \how is it possible, (in the case of the

sensation of red), to speak of the paths of reexes?" Only to answer, \It is possible,

because though we do not know what is going on in the excited nerves, muscles or

brain centers, we cannot but see the laws of pure reex and cannot but consider them

true . . .we can say that the nature of the given conscious act of man is the same as

that of the reexes".

An explicit example of the complex behavior generated by a relatively simple

reex circuit is that found in the enteric nervous system. Associated with the gas-

trointestinal tract, it is comprised of a similar number of neurons as the spinal cord

(Furness & Costa, 1980). Within it, several types of neuromuscular activity are

autonomously controlled by intrinsic sensory neurons (Bulbring et al., 1958). They

include, stationary contractions associated with segmentation (Cannon, 1902), and

two types of reex (Cannon, 1911); one a slowly advancing contraction, the other a

\peristaltic rush" which propagates rapidly.


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Numerical simulations have shown the circuit underlying this reex is sucient to

replicate both stationary and peristaltic activity, with the neuromuscular response

determined by the state of intestinal contents (gas, liquid, solid), i.e., the details of

the stimulus (Coop & Redman, 1992). These results suggest that more complex reex

circuits within other neural systems can reliably generate a range of seemingly plastic

behaviors in response to the specic details of circuit activation. Here, it is only

necessary to mention the \absent minded" week end drive resulting in unexpected

arrival at the workplace to recognize the ability of subconsciously active and entirely

learned reex pathways to formulate, control and sustain extended patterns of

complex behavior.

On the basis of the long tradition briey reviewed here, we consider that a ma-

jority of fundamental CNS operations are essentially reexive. Further, as reviewed

above, it is their reexive nature which renders their activity unconscious. In this

domain, equivalent stimuli reliably generate equivalent responses, modulated by

circumstance, where subtle dierences in circuit activation may evoke either nely

graded or signicantly dierent output.

Phylogenetic elaboration of the CNS, particularly within associative cortex

(Buckner & Krienen, 2013), results in both increased temporal separation between

reex pathway activation and response, and increased complexity of learned reexive

behavior; with (as we propose above) all such reexive activity constrained to the

subconscious. Ultimately, as Velmans (2009) has put it, \an entity in the world is

reexively experienced to be an entity in the world".

In summary, Sherrington (1906) originally described the vertebrate nervous system

as an orchestrated constellation of increasingly elaborated reex pathways culmi-

nating in a head ganglion or brain. From this perspective, the known record of

vertebrate evolutionary history (see e.g., Butler (2009)), and development of the

associative circuits of the hominid nervous system (Buckner & Krienen, 2013), it is

likely appropriate inhibitory processes andmodulation of intrinsic and learned reexes

is fundamental to CNS function, and thus, ultimately, behavior and consciousness.

3.2. Inhibition and disinhibition of reexive behavior

Typically, a personmight be considered capable of expressing a near innite repertoire

of behaviors. However, it is clear that in the normal course of events, they are never all

expressed simultaneously. Rather, sequences of behavioral patterns, each appropriate

to the given circumstances, are expressed as ongoing behavioral ows generated in

response to perceived environmental concerns. The emergence of a particular behavior

from a repertoire of possible behaviors is controlled by the (psychological) repression

or (physiological) central inhibition of alternative behaviors (Beritov, 1968). This is

the basic factor providing for the integrity of behavioral reactions. Further, Beritov

(1968), reports central inhibition caused by stimulation of sensory nerves embraces

the entire neuroaxis and follows adequate stimulation of all sensory modalities. In

humans, general central inhibition also occurs during deliberate cognitive activities,


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such as arithmetic and suppression of conditioned and unconditioned reex activity.

We take this to mean that tonic inhibition at the physiological-level is responsible for

repression in the cognitive and behavioral domains.

As Smith (1992) has concluded, \Inhibition . . . became the controlling mechanism

that made possible those very functions, thought and deliberative action, that gave

humanity dignity and independence from nature. The possibility of inhibition was

the possibility that past associations rather than immediate sensations would

sometimes initiate movements. It was the possibility that sensation might combine

and recombine as intelligence and thought. Without inhibition, sensation merely

exhausted itself in movement".

Gray (2002) considers that the inhibitory function of consciousness solves a major

evolutionary problem: How to ensure that automatic responses are appropriately

activated; and how controlled processes are invoked only at critical junctures when a

denite choice must be made between cautious risk-assessment and prepotent

responses. At these moments, after ne-grained analysis aorded by control pro-

cessing, appropriate adjustments can be made to the automatic system, such that

when the same (or similar) stimuli are encountered in the future, automatic-reexive

behavior will be more appropriate. In this way, controlled/conscious eects come to

determine automatic/nonconscious eects, albeit with a time lag.

We have previously concluded that, in the electrophysiological domain, ring of

hippocampal pyramidal and cerebellar Purkinje neurons (Coop & Reeke, 2004; Coop

& Redman, 1998), may more immediately be controlled through disinhibition and

eective connectivity, than alterations in aerent stimulation frequency.

It has recently been reported frontal cortex mediates unconsciously triggered in-

hibitory control (van Gaal et al., 2008), and a role for inhibition in the control of

cortical activity is further supported by disinhibition being a signicant control

mechanism in the spinal cord (Sechenov, 1863), striatum (Chevalier & Deniau, 1990)

and somatosensory cortex (Xing & Gerstein, 1996a,b,c), including olfactory bulb

(Cazako et al., 2014). More generally, there is persuasive evidence the cortex may be

under widespread and strong inhibition (Calford & Tweedale, 1991; Dykes et al.,

1984), while pathological alterations to inhibition may lead to the excitatory dys-

functions of epilepsy (Avoli, 2004) and schizophrenia (Lewis et al., 2005). A recent

review of the functional signicance of intrinsic oscillatory brain properties con-

cluded, \it is by selection, via inhibition that the most elaborate neuronal patterns

are generated in the CNS" (Llinas, 2014).

3.3. Learning and habituation

In a recent review, Schacter et al. (2011) consider human learning to be acquisition of

knowledge or skills through experience, study, or by being taught. However, learning

is not usually immediate, but rather typically is an incremental process building

upon, and shaped by, what is already known; to produce relatively permanent

changes in the behavior of an organism.


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Two types of learnings have been distinguished (Kandel et al., 2000a). The sim-

plest is non-associative. Two forms are common, habituation (Sokolov, 1963) and

sensitization (Shettleworth, 2010). Two forms of associative learning have also been

identied, classical (Pavlov, 1927) and operant (Thorndike, 1911) conditioning.

As suggested by Sechenov (1863), learning may contribute to understanding,

knowledge and as we have seen, even qualia (where qualia have been proposed to

originate in local cortical network activity (Orpwood, 2013)), \the successive reexes

acquired by learning lead to a perfect notion of the object, to knowledge in its ele-

mentary form. Indeed, the scientic knowledge of external objects is simply an in-

nitely broad notion of each of them, i.e., the sum of all possible sensations evoked in

us by these objects under all conceivable conditions . . .I shall merely point out that

sensations from all spheres of the senses can be diversely combined, but always by

means of consecutive reexes. These combinations give rise to countless notions that

arise in childhood, notions providing, so to speak, material for the entire subsequent

psychical life".

In other words, when objects in the environment occur frequently enough, with

repeated regularities, they can be incrementally added to the memory of similar

previous encounters. Slight variations over time elaborate the memory system far

beyond that of any single sensory experience, and as Sechenov suggests, this con-

tinually enriches records of sensory experience and thus conscious phenomena.

It is notable that at the electrophysiological level, very young animals may only

receive and integrate relatively small amounts of information per unit time in circuits

which function more slowly than those of adults (Scherrer, 1968). Associated learning

may occur consciously or unconsciously. For example, the eects of internal stimuli

have been shown to be active as early as the embryonic stage, particularly in studies

of conditions under which the onset and patterning of electrical activity takes place in

the higher parts of the embryonic brain.

Even at this early stage, central inhibition displays its controlling inuence on

coordinating reex activity (Biryukov, 1968), and there is evidence for prenatal

habituation in humans as early as the 32nd week of gestation (Sandman et al., 1997),

indicating the nervous system is developed for learning and memory formation prior

to birth.

3.4. The unity of fragments of memory

The recollection of past experience is considered to be a reconstructive process. It can

be broken down into a number of constituent processes, with memories recreated

from their component parts, although little is known about the neural correlates

(Hassabis & Maguire, 2009). As such, human memory has been considered comprised

of a variety of testable components forming a \memory system"a containing past

aWe recognize the nomenclature generally accepted in memory research, where \memory system" refers to the

multistore memory model (LaRocque et al., 2014). However, for convenience we use this phrase to refer to the morestate-based or unitary memory model described by Brown et al. (2007).


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experience (Atkinson & Shiffrin, 1968). This multi-store modal memory model pro-

poses sensory memory containing short-term records of sensory stimulation (250

500ms duration). Those stimuli which are attended enter short-term memory (up to

18 s duration), and if suciently rehearsed are transferred to long-term memory (in

principle unlimited).

Each of these memory domains has subsequently been further decomposed. For

example, short-term memory is associated with a working memory (Baddeley &

Hitch, 1974), while long-term memory may be divided into either explicit memory

which is partitioned into episodic (Tulving, 1972), procedural (Milner, 1962) and

semantic (Tulving, 1972) components; or declarative memory, comprising implicit or

procedural memory (Schacter, 1987) or emotional memory (LeDoux, 2000).

One signicant problem with this multi-store approach is that dierent principles

are assumed to apply over dierent time scales. This runs counter to the generally

held expectation that scientic principles should hold over a wide range of temporal,

spatial, or physical scales (Barenblatt, 1996). As a consequence, Brown et al. (2007)

have proposed memory is unitary over all time scales, from milliseconds to years.

Here, the basic idea is that items are more distinctive, and hence both more

memorable and easier to identify, to the extent they are located in sparsely-populated

regions of psychological space. This implies forgetting is a consequence of reduced

local distinctiveness, not trace decay. Importantly, the same mechanisms are used for

retrieval over all time scales. There is considerable empirical support for this model as

it resolves many observations not easily accounted for by the more widely accepted

multi-store memory model.

This so-called temporal ratio model is concordant with the synaptic trace theory of

memory rst proposed by Hebb (1949). He posits the brain retains information

through learning-induced changes in the synaptic connections between neurons.

Once consolidated, a memory is then embedded and embodied through its xed

trace. Thus, learning occurs through general mechanisms of experience-dependent

synaptic plasticity, e.g. Hubel et al. (1977), which ultimately lead through a cascade

of intracellular molecular mechanisms to the formation of long-term memory. Sub-

sequently, it has been shown memories can temporarily be rendered labile and sen-

sitive to modication. Once an existing memory has been destabilized, it is possible to

enhance and even incorporate new content (for review, see Flavell et al. (2014)).

For over a century, psychologists have focused their studies on memory of the past.

However, a signicant function of memory is its role in allowing individuals to imagine

possible future events (Schacter et al., 2007), to guide behavior in the future based on

analogies, through memory resulting from both real and imagined experience (Bar,

2009b). Schacter & Addis (2009) consider that predicting the future and remembering

the past may be more closely related than everyday experience suggests. It has re-

cently been shown that similarities in cognitive processes underlying past and future

events are complemented by analogous similarities in brain activity. For example, the

same \core network" of brain regions is recruited when people remember the past and

imagine the future (Buckner et al., 2008; Schacter et al., 2008, 2007).


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In this view, past and future events draw on similar information stored in memory

and rely on similar underlying processes: in an active creative extrapolation, memory

supports the construction of future events by extracting and recombining stored

information into a simulation of a novel event. Schacter et al. (2008) further suggest

that simulation of future events requires a system that can exibly recombine details

from past events. Thus, memory can be thought of as a tool used by the prospective

brain to generate simulations of possible future events. Schacter et al. (2007) consider

such a hypothesis requires a shift of conceptual emphasis with regard to the role of

memory in cerebral activity.

3.5. Prediction as reconstruction of the future

Prediction is pervasive throughout much of brain function and is almost continually

operative at conscious and reex-levels, as success in a goal-oriented, moving system

is enhanced by such innate functionality (Llinas, 2001). For the nervous system to

predict, it must at least perform a rapid comparison of the sensory-referred properties

of the external world with a separate internal sensorimotor representation of those

properties (Llinas & Roy, 2009).

If it is to synchronize with the external events of each given moment the brain

must leave itself enough time to implement movement decisions. It cannot be stuck

doing something when required to perform another task. The consequent mode of

operation derives from a \look-ahead function", proposed to be an inherent property

of neural circuits (Llinas, 2001).

Pellionisz & Llinas (1979) provide a model of such a function based on the Taylor

expansion. It yields predictions of the frequency-time function of cortical input and is

an emergent property of inherently parallel distributed neural circuits. It relies on

relationships between neuronal ring rates and events in the external world. If some

neurons respond quickly, some do so at intermediate velocities, and some measure

events in real time, the output of such a circuit will be a reconstruction or prediction

of an event ahead of its time of completion. It is widely believed, in the absence of any

other possible sources, such functionality is memory-based (Bar, 2009a).

The signicance of such a mechanism is found mainly by its incorporation into

larger, cognitive states or entities. In other words, the extent to which sensory cues

aect brain function is determined by their impact upon pre-existing functional

dispositions of the brain (Llinas, 1987, 1974). Llinas (2001) considers this indicates a

far deeper issue than might initially appear. In fact, the predictive abilities of the

brain may be profoundly more fundamental than suggested by a purely look-ahead

model.

We extend this approach to provide a signicantly more comprehensive predictive

functionality which lies at the heart of the aerence copy model. It is distinguished by

originating entirely within the memory system, an absence of immediately direct

comparison between sensory-referred properties of the external world and internal

sensorimotor correlates, and provision of a basis for conscious temporal detachment.


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In fact, we claim that through infant learning, physiological processes of aerence

copy are evoked as sets of embedded reex functions. They lead to the creation of

temporal experience and consciousness through their ability to fabricate the phe-

nomena of the present moment. The correlate is development of an awareness which

enables distinction of the past from the future and thereby create the subjective

temporal experience and phenomenology of each given moment.

3.6. Estimates of memory capacity and rate of formation

Unquantied beliefs concerning the characteristics of the human brain have long

been considered to make it an outlier in evolutionary terms and are frequently

employed to justify its remarkable cognitive abilities. However, the human brain has

been found to contain just the number of neurons and non-neuronal cells expected for

a primate brain of its size; with the same distribution of neurons between its cerebral

cortex and cerebellum as in other species, along with appropriately scaled energy

costs (Herculano-Houzel, 2011, 2012).

In concordance with our identication of a putative aerence copy system, in this

section we take the opportunity to provide some estimates of what might be referred

to as the content acquisition and content storage domains of the human CNS. These

may be distinguished from the content manipulation domain.

With regard to content manipulation, there is a considerable literature reporting

estimates of the transmission rate of information by neurons within the CNS. These

estimates are typically based on an assumption of either a rate or temporal code.

Theoretically, for a rate code with strictly periodic neuronal ring, the information

per spike is calculated from log2N=N , where N gives the number of spikes persecond. This gives values of 3:3 101 and 6:6 102 bits spike1 for ring rates of10 and 100 spikes s1, respectively. Alternatively, for a temporal code, where thevariability of spike timing is taken into account, the calculation of information

transmission becomes considerably more complicated (e.g., see Stein (1967)). In

short, for example, information per spike increases to 34 bits spike1 (Softky,1995), with a theoretical maximum of about 9 bits spike1 (MacKay & McCulloch,1952).

However, here we are initially interested in the content storage domain of the

memory system, in particular, an estimate of its \storage capacity". Such an estimate

then allows a \mean acquisition rate" to be determined for the content acquisition

domain. In doing this we are estimating a possible rate at which experience may be

recorded prior to transformation to states of the nervous system within the content

manipulation and storage domains.

One way to quantify these domains is in computational terms. For example, a

synapse can be represented as a single binary bit. Based on this assumption we can

employ the following data to make an \order of magnitude" estimate of storage

capacity. The aim is to give some sense of the putative capacity of human memory

in computational terms. We note, better estimates will be considerably complicated


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by, for example, neuronal loss due to ageing in the frontal lobes (up to 20%

(Masliah et al., 1993; Gibson, 1983)), and likely continual addition of neurons in,

at least, the hippocampus (Altman, 1963), olfactory bulb (Altman, 1969) and

striatum (Ernst et al., 2014).

The human brain has been reported to contain 86:1 109 8:1 109 neurons,of which 19%, or approximately 16:4 109 are cortically located (Azevedo et al.,2009). The number of synapses in the neocortex has been reported at 1:5 1014(Pakkenberg et al., 2003). Assuming non-cortical neurons exhibit a similar average

number of synapses as cortical neurons, and all synapses may be modied by expe-

rience; the total estimated number of synapses in the brain may be as large as

7:89 1014.At one bit per synapse, this number of synapses corresponds to a storage capacity

of about 90Tb. Assuming a human lifespan of 70 years, with the knowledge there are

approximately 3:2 1010 ms in a year, it can be estimated there are on average about358 \naive" synapses available each millisecond to record the state of the nervous

system. From a computational perspective, this corresponds to storage of

44 bytesms1 or 43Kb s1, 2.5Mbminute1, 150Mbhour1 or 3.5Gb day1. Thisdaily value is comparable with high denition movies which consume approximately

2Gbhour1. Interestingly, by this analysis, a 90min movie has a similar storagerequirement to our estimate of the average daily human storage capacity.

These gures may signicantly increase if it is accepted that new memories cannot

be formed during sleep, which is considered to be reserved for the stabilization,

enhancement and integration of memories (Walker et al., 2005). If it is assumed on

average a person spends approximately 8 h sleeping each day, then memory storage

capacity may increase up to about 470 synapses per millisecond, corresponding to

storage throughout waking life of 57.3Kb s1 or approximately 200Mbhour1.From a computational perspective, such calculations provide an indication of the

general volumes of \data storage" or average sustainable daily rate of lifetime

memory formation and provide a starting point for the development of more practical

hypotheses. Although the putative per millisecond synaptic sampling rate seems

trivial, as our calculations show, the cumulative capacity is substantial. As Sechenov

(1863) has proposed, \By means of absolutely involuntary learning . . . in all spheres

of the senses the child acquires a multitude of more or less complete ideas of objects,

i.e., elementary concrete knowledge".

4. The Explanatory Gap

The \explanatory gap" is a philosophical term referring to the lack of an explanation

of how physical properties give rise to the qualia of experience (Levine, 1983). We

appreciate such a \literary" denition is a necessary step in problem identication,

but consider it a misplaced expectation that any deep resolution is possible while

explication languishes in such purely metaphorical or narrative domains. Any solu-

tion is likely only available following location of the \gap" within an appropriate


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neuropsychophysiological context. More specically, we consider the problem of the

explanatory gap becomes tractable when translated from a philosophical to an em-

pirical context.

Quantication is fundamental to the scientic method and by making this con-

ceptual transformation, the philosophical idea of the explanatory gap can be placed

rmly into the core of the scientic tradition. However, we recognize that with

quantication comes reduction, itself a characteristic of the scientic method. In doing

so we acknowledge the metaphorical nature of much written about consciousness. As

suggested in the Introduction, because of the highly multidimensional, intangible and

generally elusive nature of consciousness many of its various aspects are only available

through metaphorical language and description. It is these aspects which are greatly

reduced by transference from the philosophical to the physiological domain.

To make this transfer we propose, at its most general, that the physiological

explanatory gap is dened as the gap between the occurrence of a stimulus at ex-

ternally or internally directed sensory receptors and the initiation of a response,

motor or otherwise. It is this gap which must be \explained" by the nervous system

and to which, in its own way, aspects of the philosophical formulation actually refer.

Most importantly, during this period it is not possible for a nervous system to

know anything about changes in the external environment. For this reason, a sig-

nicant evolutionary advantage likely accrues to an organism capable of correctly

predicting evolution of the environment during this period. More specically, in the

case of placental mammals, the foregoing denition might be recast as, \the temporal

duration from the time of interaction of a sucient sensory stimulus with a receptor

until the time at which a percept of that event is subjectively recognized within

conscious experience".

This transformation recasts the problem of the explanatory gap by removing it

from a philosophical domain of narrative contemplation to the domain of empirical

quantication. There it can be rigorously studied as an incontrovertible feature of the

vertebrate CNS.

As we show below, this is an illuminating example of how narrative language used

to speculate about the brain can be recast in empirical terms to more decisively

explore CNS activity and, in this case, \bridge" the explanatory gap.

5. Eerence Copy as Motor Predictor Model

Modern eerence copy models (Fig. 1(a)) derive from a proposal which originally

posited direct sensation of the motor command: \The impulse to move, which we

initiate through the innervation of our motor nerves, is immediately perceptible".

(von Helmholtz, 1878/1971). This idea was later integrated into motor physiology

through \corollary discharge" (von Holst, 1954; Sperry, 1950).

As reviewed by Mulliken & Andersen (2009), because sensory information is

substantially delayed, it has been proposed the brain makes use of an internal for-

ward model which relies on eerence or eerent copy. This is an internal copy of an


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outowing, movement-producing signal generated by the motor system. It is pro-

posed to allow integration of sensory and motor feedback signals to estimate current

and upcoming positions and motions of a limb during movement (Blakemore et al.,

2000). Upon eective execution, the actual proprioceptive feedback of a motor action

eectively balances the predicted sensory feedback. Thereby, the eerence copy is an

early-warning signal sent by motor production areas to the corresponding somato-

sensory areas specialized in the proprioception of motor execution. It also allows

perceptual structures to distinguish between self and externally mediated signals.

6. Aerence Copy as Sensory Predictor Model

An explanatory gap exists for the time it takes a sensory stimulus to evoke fabri-

cation of a current percept and for the percept to emerge into consciousness. Our

claim is, this physiological explanatory gap is bridged by conscious experience, which

originates through aerence copy as a construct evoked from within the memory

system.

The special character of this consciously experienced percept is that it is not

actually just a record of sensory activation entering the nervous system. Rather, it is

a memory-based prediction (activated by stimulus presence) of the state of the

internal and external environment of the nervous system expected at the time

(a) (b)

Fig. 1. A. Eerence Copy: Model proposes that upon motor preparation and intention, copies ofeerent motor information are fed back and used centrally in an emulation algorithm, which calculatesthe anticipated somatosensory changes expected as a consequence of the planned motor execution.Subsequently, peripheral changes at the level of the muscles, the joints and the skin generate actualproprioceptive feedback, which will eectively balance the predicted sensory feedback in somatosensorycortex (at the level of a so-called \comparator"). B. Aerence copy: A model complementary to eerencecopy proposes that upon sensory stimulation, receptor stimuli are fed forward and maintained sub-consciously in the memory system while they are integrated with the relevant memories they evoke.Once integration is complete, a prediction of the percept expected on the basis of the received sensorystimulus emerges as an \aerence copy" into the explanatory gap created by the time taken for inte-gration to occur. If the aerence copy eectively matches the environment, predicted experience andactual experience match suciently that no further action is required. Otherwise, surprise is experiencedand attention may be redirected. Panel A adapted from (Bazan, 2012).


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integration of the given sensory input is complete. It is in this sense that aerence

copy is a predictor of sensory experience. This process is illustrated and explained in

more detail in Fig. 2.

Aerence copy can be conceptualized as complementary to the eerence copy

system (Fig. 1(b)), but applied to inowing sensory activation rather than the out-

owing, movement-producing activity of the motor system. It is the physiological

mechanism which enables and completes the cyclic ow of experience and behavior

through the cognitive domain of the nervous system and the physical world within

which it is embedded.

Following, for example, Dehaene & Naccache (2001) and Gray (2004), it is clear

the neural activity driving aerence copy is widely distributed, although the details

of precise location and mechanism are as yet unclear. Nevertheless, in the normal

course of events, the construct fabricated by aerence copy processes would be based

on, and exist in, the \past" due to the temporal delay introduced by the neural

activity enabling its conscious appearance. This situation is only compounded by the

fact that each successive moment is also a past moment prior to being experienced as

the present.

The aerence copy model is proposed as a solution as to how it is that subjective

experience appears to exist in the present moment when the time required for sen-

sations to consciously appear necessarily require sensory events evoking a conscious

percept to occur in the past.

The model resolves this apparent conict in the following way. At any one mo-

ment, entry of sensory input into consciousness is delayed while its eects are inte-

grated into ongoing neural activity to fabricate withinb the memory system a

comprehensive percept of the contents expected or predicted for a given moment.

Importantly, we further claim that the ability to do this is learned, as is the

content of the behavioral repertoire it ultimately subserves, with the complexity of

the processes involved being a major reason for the extended developmental period

seen in humans. As they are learned, the processes subserving aerence copy, simi-

larly to other learning, become a \reexive" mechanism residing in the subconscious.

It is in this way the explanatory gap is bridged and conscious experience gener-

ated. The content of consciousness is this memory-based prediction of the composi-

tion of the next actual future moment, subjectively experienced as the present

moment. It is a reexive mechanism learned during development to accommodate

ongoing function in the ubiquitous presence of the explanatory gap.

Ultimately, ongoing neural activity is modulated as required by sensory content

and the associations it evokes from within the memory system. What is commonly

referred to and experienced as subjective phenomenal consciousness is this

bIt does not make sense to say \from" memory as this implies memory is consulted by some lookup procedure. This

creates a signicant problem as retrieved content must be collected and displayed somewhere. Attempts to resolve

this additional complexity has spurred previous solutions resulting in homunculi and the mechanics of the Cartesian

Theatre. Importantly, following Nikoli (2014), we consider \monitor-and-act" is a more complete descriptor thanthe notion of representation as the former incorporates both \memory storage" and \processing".


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Fig. 2. Framework for consciousness: The schema is given for a single external stimulus. Model fea-tures are given at the top (A. Explanatory gap, C. Predicted percept) and subjective time (Past mo-ment, Present moment, Future moment) indicated at the bottom of each panel for three consecutive550ms moments (separated by dark vertical bars). Upper horizontal dotted line distinguishes twodomains within each panel. An upper physical domain contains a stimulus originating externally to thenervous system. A lower cognitive domain (within the nervous system) is further subdivided into two\internal" domains; a sub/pre-conscious domain (top) containing the memory system (comprisingsensory, short and long-term memory); and a conscious domain (bottom). Stimulus evoked sensoryarousal activates the memory system () to evoke relevant memories of previous stimulus experiencewhich together are integrated (! ) to generate an appropriately fabricated percept then released tothe conscious domain () as the best prediction of immediate future experience. Panel 1: An Explana-tory gap 1A exists in the past moment (1B) for the time it takes (! ) a stimulus to evoke acomprehensive prediction within the memory system of future stimulus-modulated experience. Oncefabricated, the Predicted percept (1C) emerges into the conscious domain (indicated by vertical stripesprojecting from the sub/preconscious domain into the conscious domain and perception) as a subjectiveconscious experience in the Present moment (1D). The large upper arrow head indicates appropriateongoing subconscious elaboration of memory by incorporation of correctly predicted perceptual com-ponents. The large lower arrow indicates the ongoing evolution of predicted perceptual experiencewithin the conscious domain. Panel 2: Illustrates temporal evolution of the relationships given in Panel 1into the next moments. During the Explanatory gap (2A), integration of a new sensory stimulus nowoccurs within memory system while the predicted percept generated during the explanatory gap of the(just passed) moment (1B) has now emerged as an appropriate stimulus modulated percept into theconscious domain of the present moment (illustrated in 1D, but for clarity not shown in 2B). Thisprocess continues as the Predicted percept (2C) being generated during the current Explanatory gap(2A) will be consciously experienced in the subsequent Future moment (2D). It is in this way ongoingperceptual experience is continuously generated through aerence copy to bridge the sliding window ofthe explanatory gap. Consciously experienced subjective phenomenology is a product of a previouslyconstructed prediction of the experiential contents expected to occur during the present moment.


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physiological process of creating a prediction of the experience of the present moment

based on prior experience of the given situation or environment.

When this functionality is paired with the ability of the CNS and itsmemory system

to discriminate and cumulatively \record" in the domain of single photons (Gregory,

1966) and atoms (Green, 1976); the elements available for fabrication create eectively

\seamless" and entirely \resolvable" percepts. Naturally, environmental needs and

requirements create

Afference copy as a quantitative neurophysiological model for consciousness

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