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C H A P T E R

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The Neuroscience of Consciousness

Consciousness is one of the most enigmatic features of
the universe. People—and presumably many other animals, too—not only act but feel: they see, hear, smell,
recall, plan for the future. These activities are associated
with subjective, ineffable, immaterial feelings that are tied
in some manner to the material brain. The exact nature of
this relationship—the classical mind-body problem—
remains elusive and the subject of heated debate. These
firsthand, subjective experiences pose a daunting challenge to the scientific method that has, in many other
areas, proven so immensely fruitful. Science can describe
events microseconds following the Big Bang, offer an
increasingly detailed account of matter and how to manipulate it, and uncover the biophysical and neurophysiological nuts and bolts of the brain and its pathologies.
However, this same method has as yet failed to provide
a satisfactory account of how firsthand, subjective experience fits into the objective, physical universe. The brute
fact of consciousness comes as a total surprise; it does
not appear to follow from any phenomena in physics or
biology. Indeed, some modern philosophers argue that
consciousness is not logically supervenient to physics
(Chalmers, 1996). That is, it is certainly logically possible
to imagine a world identical to ours but without any
conscious experience. Nothing in the known laws of
physics—or of biology—seems to contradict this. Yet we
do find ourselves in a world where each one of us has conscious experiences, sees a picture of the world and so on.
People willingly concede that when it comes to nuclear
physics or molecular biology, specialist knowledge is
essential; but many assume that there are few relevant
facts about consciousness and therefore everybody is
entitled to their own theory. Nothing could be further
from the truth. There is an immense amount of relevant
psychological, clinical, and neuroscientific data and

Fundamental Neuroscience, Fourth Edition. DOI: 10.1016/B978-0-12-385870-2.00051-2

observations that must be accounted for. Furthermore,
the modern focus on the neuronal basis of consciousness
in the brain—rather than on interminable philosophical
debates—has given brain scientists tools to greatly
increase our knowledge of the conscious mind.
Consciousness is a state-dependent property of certain
types of complex, biological, adaptive, and highly interconnected systems. The best example of consciousness is
found in a healthy and attentive human brain—for example, the reader of this chapter. Not all biological, adaptive
systems appear to have consciousness; examples include
the enteric nervous system and the immune system. Brain
scientists are exploiting a number of empirical approaches
that shed light on the neural basis of consciousness. This
chapter reviews these approaches and summarizes what
has been learned.

WHAT PHENOMENA DOES
CONSCIOUSNESS ENCOMPASS?
There are many definitions of consciousness (Searle,
2004). A common philosophical one is “Consciousness is
what it is like to be something,” such as the experience of what
it feels like to see red, to be me, or to be angry. This what-itfeels-like-from-within definition expresses the principal
irreducible characteristic of the phenomenal aspect of
consciousness: to experience something. “What it feels like
to see red” also emphasizes the subjective or first-person
perspective of consciousness: it is a subject, an I, who is
having the experiences, and the experience is inevitably
private.
A science of consciousness must explain the exact
relationship between phenomenal, mental states, and
brain states. This is the heart of the classical mind-body

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Why? Furthermore. why does any one brain state—that is.. what psychologists call the feeling of agency or authorship (e. 2008). Why are only some behaviors associated with conscious states? Much brain activity and associated behavior occur without any conscious sensation. 1996). 3. What is the function—if any—of conscious experiences? THE NEUROBIOLOGY OF FREE WILL A further aspect of the mind-body problem is the question of free will. tracking a spot of light moving every 2. 2008. scientific explanation. In other words. Haggard. This temporal marker for the awareness of willing an action occurs on average 200 msec before initiation of muscular action (with a standard error of about 20 msec). a vast topic. THE NEUROSCIENCE OF CONSCIOUSNESS problem: What is the nature of the relationship between the immaterial. In other words.56 seconds around a circle. cyan. If this action is repeated sufficiently often while electrical activity around the vertex of the head is recorded. because of its counterintuitive implication that conscious will has no causal role. or color to an achromat—rare individuals born without any cone photoreceptors. red. the interpretation of these experiments continues to be vigorously debated (Haggard. 5. under different circumstances. 4. without an adequate reductionistic. and magenta are all colors that can be mapped onto the topology of a circle. Yet whether volition is illusory or is free in some libertarian sense does not answer the question of how subjective states relate to brain states. BEHAVIORAL AND COGNITIVE NEUROSCIENCE . this is referred to by some as the Hard Problem (note the capitalization). Of great relevance are the classical findings by Libet.” the subject had to carry out a specific voluntary action. and Pearl (1983) of brain events that precede the conscious initiation of a voluntary action. Every now and then. we cannot communicate an experience to somebody else except by way of example. 2008). where precentral and parietal cortices can signal decisions up to ten seconds prior to entering awareness. So even if free will is a complete chimera. “spontaneously. here flexing their wrist. Libet asked subjects to silently note the position of the spot of light when they first “felt the urge” to flex their wrist and to report this location afterward. Why is the relationship among different experiences the way it is? For instance. These implicate posterior parietal. Many scholars have argued that the exact nature of this relationship will remain a central puzzle of human existence. these color percepts share certain commonalities that make them different from other percepts. in accordance with commonsense notions of the causal action of free will. neurons over here firing. is a subjective state with an associated quale no different in kind from the quale of a toothache or seeing marine blue. it is best to put this question aside for the moment and not be taken in by defeatist arguments. the subject’s brain signals the action at least half a second before the subject feels that he or she has initiated it! The original experiment has been replicated (Haggard & Eimer. 2009. the neural correlate for the feeling of apparent causation involves activity in these regions. “I decided to lift my finger”). phenomenal world (Chalmers. objective world and the subjective. The perception of free will. Why is there any experience at all? Or. 1999) as well as extended using fMRI. subjects were sitting in front of an oscilloscope. Psychological work in normal individuals and in patients reveals further dissociations between the conscious perception of a willed action and its actual execution: subjects believe that they perform actions that they did not do. blue. The quiddity of the sensation of agency has been strengthened by direct electrical brain stimulation during neurosurgery and fMRI experiments. Think of the unmistakable smell of dogs coming in from the rain or the crunchy texture of potato chips. However. The spectrum of views ranges from the traditional and deeply embedded belief that we are free. medial pre-motor and anterior cingulate cortices in generating the subjective feeling of triggering an action (Desmurgert et al. 2. the readiness potential can be detected at least 350 msec before awareness of the action. Answering this question goes to the heart of the way people think of themselves. put differently. Yet. while neurons over there remain silent— feel like anything? In philosophy. subjects feel that they are not responsible for actions that are.1092 51. 2002). 6. demonstrably. a readiness potential (Bereitschaftspotential) in the form of a sustained scalp negativity develops 1–2 sec before the muscle starts to move. Why are feelings private? As expressed by poets and novelists. or as the explanatory gap between the material. yellow. In this seminal experiment. while. and conscious actors to the view that we are biological machines driven by needs and desires beyond conscious access and with limited insight or voluntary control. such as seeing motion or smelling a rose. the subjective feeling of willing an action must have some neuronal correlate. as a group. However. VII. conscious mind and its physical basis in the electrochemical interactions in the body? This problem can be divided into several subproblems: 1. Wright. green. autonomous. Gleason. as similar sentiments have been expressed in the past for the problem of seeking to understand life or to determine what material the stars are made out of.g. Try explaining vision to somebody blind from birth. their own (Haggard. Wegner. How do feelings acquire meaning? Subjective states are not abstract states but have an immense amount of associated explicit and implicit feelings..

olfactory. and other birds. such as tuna. fluctuates in a circadian manner. They are not the same and obey slightly different anatomical scaling laws but are overall remarkably similar (Herculano-Houzel. and is influenced by lack of sleep. it is unclear where in the animal kingdom to draw the Rubicon that separates species with at least some conscious percepts from those that never experience anything and that are nothing but pure automata (Edelman. drugs and alcohol. There are three reasons to assume that many species. non-matching-to-sample. Zhang. & Srinivasan. monkeys. 2005. pain. in particular those with complex behaviors such as mammals. cellular. avoidance behaviors at the prospect of a repetition of the painful stimulus—can be observed in all mammals and in many other species.AROUSAL AND STATES OF CONSCIOUSNESS CONSCIOUSNESS IN OTHER SPECIES Data about subjective states come not only from people who can talk about their subjective experiences but also from nonlinguistic competent individuals—such as newborn babies or patients with complete paralysis of nearly all voluntary muscles (locked-in syndrome)—and. 2. parrots. Similar behavior: Almost all human behaviors have precursors in the animal literature. happiness.. BEHAVIORAL AND COGNITIVE NEUROSCIENCE . motor activity such as writhing. a belief with no empirical basis. or even invertebrates. Homo sapiens is part of an evolutionary continuum with its implied structural and behavioral continuity. The discovery of cortical pain responses in premature babies (Slater et al. nonstereotyped behaviors including delayed-matching. the sound level necessary to evoke an eye movement or a head turn toward the sound source). & Seth. about 60 million years ago. crows. remembered or imagined experiences. resulting in change in blood pressure. increased heart rate. and whales. VII. The behaviors seen in humans when they experience pain and distress—facial contortions. Similar neuronal architecture: Except for size. from animals other than humans. it is not clear whether one can be awake without being conscious of something (with the possible exception of certain meditative states). This is as true of wakefulness as it is of REM sleep that can be vividly. relating to the intransitive and to the transitive usage of the verb. physical exertion. about 220 million years ago. and other forms of learning (Giurfa. there are no large-scale genomic. moaning. surprise. Koch. yelping. in particular those relating to the self. or memory—that has a specific content. 2012). measured by electrical or metabolic brain activity. such as squids or bees. The level of brain arousal. AROUSAL AND STATES OF CONSCIOUSNESS There are two quite distinct meanings of being conscious. are singled out by the gift of consciousness above all other species. To believe that humans are special. Referring to such conscious states is conceptually quite distinct from referring to states of consciousness that fluctuate with different levels of arousal. ravens. remember an incident. is a remnant of humanity’s atavistic. share at least some aspects of consciousness with humans: 1. most importantly. The former revolves around arousal and states of consciousness. Evolutionary continuity: The first true mammals appeared at the end of the Triassic period. Arousal can be measured behaviorally by the signal amplitude that triggers some criterion reaction (for instance. release of stress hormones. visceral. the brain must be in a relatively high state of arousal.. and emotional experiences (fear. Jenett. Baars. To be conscious of anything. cichlid. vestibular. High arousal states are always associated with some conscious state—a percept. with primates proliferating following the Cretaceous-Tertiary extinction event. magpies. and so on). while humans and macaque monkeys did not diverge until 30 million years ago (Allman. 2006) and of empathy and observational pain in mice (Jeon et al. sweating. deeply held belief that 1093 Homo sapiens occupies a privileged place in the universe. Without a sounder understanding of the neuronal architecture necessary to support consciousness. 2001) are conscious is difficult to answer at this point in time. culturally transmitted knowledge. 2010) shows the fallacy of relying on language as sole criteria for consciousness. with complex. or fantasize about sex. dilated pupils. The number of distinct conscious states is vast and encompasses every possible type of visual. and other fish. humans. Indeed. there is little reason to doubt that other mammals share conscious feelings—sentience—with humans. Take the case of pain. The extent to which nonmammalian vertebrates. dread. or neurophysiological differences between the cerebral cortex and thalamus of mice. While certain aspects of consciousness. We see and hear something. 3. thought. events or thoughts. rather than an independently developed organism. or other forms of vocalization. auditory. 1999). consciously experienced—though usually not remembered—in dreams (see Chapter 40). may not be widespread in nonhuman animals. 2009). and so on in a predictable manner. Menzel. or other sensory experience. plan the future. architectonic. introspection and to abstract. and so on. Likewise for the physiological signals that attend pain—activation of the sympathetic autonomous nervous system. while the latter deals with the content of consciousness and conscious states.

2010). since no color. or depth could be perceived or imagined. Increasing levels of behaviorally determined arousal are plotted on the x-axis and the “richness” or “representational capacity of consciousness” is plotted on the y-axis. BEHAVIORAL AND COGNITIVE NEUROSCIENCE . paradoxically. the loss of integration within the cortico-thalamic core. and the subject is difficult to wake up. Tononi. VS. complex partial seizures MCS Level of arousal Brain Coma PVS death FIGURE 51. Two empirico-computational assays being developed rely on the breakdown of cortico-cortical interconnectivity—that is. and sporadic sensory percepts)..1 Normal and pathological brain states can be situated in a two-dimensional graph. to a fluctuating and limited form of conscious sensation in MCS. vivid states. 2005. by differential eye movements) and who shows some signs of consciousness. or general anesthesia.1) in which the richness of conscious experience (its representational capacity) is plotted as a function of levels of behavioral arousal or responsiveness. Modified from Laureys (2005). low levels of behavioral arousal go hand-in-hand with vivid consciousness. Brain imaging of patients with global disturbances of consciousness (including akinetic mutism) reveals that dysfunction in a widespread cortical network including medial and lateral prefrontal cortex and parietal associative areas is associated with a global loss of consciousness (Laureys. Conversely. affecting the space of possible conscious experiences.. 2011. the origin of this space has been reached with no experience at all (Fig.g. These observations suggest a two-dimensional graph (Fig. Massimini et al. Monti et al. the basic physiology of the brain is changed. during which the patient should not experience anything so as to avoid traumatic memories and their undesirable sequelae. The normal. Here. after taking psychedelic drugs. 51.. inactivating all of the visual cortex in an otherwise normal individual would significantly reduce the dimensionality of conscious experience. Schiff. or during a complex partial epileptic seizure (Laureys. The repertoire of distinct conscious states or experiences that are accessible to a patient in MCS is presumably minimal (possibly including pain. More relevant to clinical practice is the case of global anesthesia. motion. the richness of conscious experience increases as an individual transitions from deep sleep to drowsiness to full wakefulness. discomfort. Given the absence of any accepted theory for the minimal neuronal criteria necessary for consciousness. For example. so does the range and complexity of behaviors that an individual is capable of. 2005. waking state is quite different from the dreaming state (for instance.” “the vegetative state” (VS). Clinicians speak of impaired states of consciousness as in “the comatose state. the latter has little or no self-reflection) or from deep sleep. 2008). when events often have a stronger emotional connotation than in normal life. In all three cases. 2012). Yet this low level of behavioral arousal goes. sleepwalking. state refers to different levels of consciousness. THE NEUROSCIENCE OF CONSCIOUSNESS Different levels or states of consciousness are associated with different kinds of conscious experiences. texture. This drives the need for practical. immeasurably smaller than the possible conscious states that can be experienced by a healthy brain. spatial orientation to a sound). from a total absence in the case of coma. and the “minimal conscious state” (MCS).1). In REM sleep. This richness of possible conscious experience could be quantified using notions from complexity theory that incorporate both the dimensionality as well as the granularity of conscious experience (e.. various pathologies of clinical relevance are associated with little to no conscious content. associated with loss of consciousness (Boly et al. Rosanova et al. In some obvious but difficult to rigorously define manner. hand in hand with high metabolic and electrical brain activity and conscious. A singular exception to this progression is REM sleep where most motor activity is shut down in the atonia that is characteristic of this phase of sleep. An alternative is blood-oxygen-level-dependent (BOLD) functional magnetic resonance imaging (fMRI). 2005).51. (2010) imaged brain activity in 54 patients VII. Global disorders of consciousness can likewise be mapped onto this plane. Physiology is also different in altered states of consciousness—for instance. Healthy subjects cycle during a 24-hour period from deep sleep with low arousal and very little conscious experience to increasing levels of arousal and conscious sensation. Representational capacity of consciousness (φ) 1094 Conscious wakefullness REM sleep Drowsiness Deep sleep General anesthesia Sleepwalking. can be difficult in a clinical setting. As behavioral arousal increases. shape. bedside tests. 51. the distinction between a VS patient—who shows regular sleep-wave transitions and who may be able to move eyes or limbs or smile in a reflexive manner as in the widely publicized 2005 case of Terri Schiavo in Florida—and a MCS patient who can communicate (on occasion) in a meaningful manner (for instance. Increasing arousal can be measured by the threshold to obtain some specific behavior (for instance. In the limit of brain death.

These receive input from many brainstem nuclei and from frontal cortex and project strongly to the basal ganglia and.2 Midline structures in the brainstem and thalamus necessary to regulate the level of brain arousal include the intralaminar nuclei of the thalamus (ILN). In summary. the thalamic reticular nucleus (NRT) encapsulating the dorsal thalamus.1095 AROUSAL AND STATES OF CONSCIOUSNESS Parietal cortex Frontal cortex Occipital cortex Thalam us ILN Medial septal nucleus Temporal cortex ste m Basal nucleus NRT of meynert ain Hypothalamus Br with disorders of consciousness to determine whether two different mental imagery tasks that involve different brain systems (“imagine playing tennis” versus “imagine navigating through your home”) can be used by the patient to communicate yes or no answers to simple questions. hippocampus. Destruction of circumscribed parts of the cerebral cortex can eliminate very specific aspects of consciousness. brainstem and basal forebrain cholinergic cells innervate the thalamus. BEHAVIORAL AND COGNITIVE NEUROSCIENCE . Acute lesions in the reticular activating system can result in loss of consciousness and coma. claustrum. and the basal ganglia. Five of these patients with traumatic brain injuries could willfully and reliably modulate their brain activity. and the midbrain reticular formation (MRF) that includes the reticular activating system. In general. Alzheimer’s disease. Small. where release of acetylcholine facilitates thalamo-cortical relay cells and suppresses inhibitory interneurons. and pons must function for the brain of an individual to be sufficiently aroused to experience anything at all. Another enabling factor for consciousness is the five or more intralaminar nuclei of the thalamus (ILN). and other forms of dementia. major cholinergic pathways originate in the brainstem and in the basal forebrain (Fig. including the amygdala. Consider the heterogeneous collection of more than 20 (on each side) nuclei in the upper brainstem (pons. increasing levels of spiking activity in cholinergic neurons are associated with wakefulness or REM sleep. into layer I of much of neocortex. It is likely that the specific content of any one conscious sensation is mediated by neurons in cortex and their associated satellite structures. serotonin. 51. and neocortex. These nuclei belong to the enabling factors for consciousness. without a concomitant loss of consciousness or even conscious vision in general. amygdala. as well as the general level of both behavioral and brain arousal. a plethora of nuclei with distinct chemical signatures in the thalamus. then acetylcholine is the most likely candidate. This shows the promise of fMRI for establishing a two-way radio link (albeit at a very low baud rate) with a subset of VS patients. If a single substance is critical for consciousness. in a more distributed manner. Cholinergic activity fluctuates with the sleep-wake cycle. and orexin/hypocretin. noradrenaline/norepinephrine. such as the ability to see moving stimuli or to recognize faces. Yet relatively discrete bilateral injuries to midline (paramedian) subcortical structures can cause a complete loss of consciousness. the ILN are necessary for the state of consciousness but do not appear to be responsible for mediating specific conscious percepts or memories. cholinergic basal forebrain neurons send their axons to a wide array of target structures. Brainstem cells send an ascending projection to the thalamus.2).2) or via intermediary relays in the thalamus (below) and in the basal forebrain. Cholinergic cells are therefore well positioned to influence all of the cortex by controlling the thalamus. and in the posterior hypothalamus). midbrain. eventually the excitability of thalamus and forebrain can recover and consciousness can return (Villablanca. Collectively. Two MRF FIGURE 51. often collectively referred to as the reticular activating system (Parvizi and Damasio. However. These structures are therefore part of the enabling factors that control the level of brain arousal (as determined by metabolic or electrical activity) and that are needed for any conscious states to form. histamine. 1995). thalamus. midbrain. Thus. many neurological pathologies whose symptoms include disturbances of consciousness. In contrast. These nuclei—three-dimensional collections of neurons with their own cytoarchitecture and neurochemical identity— release distinct neuromodulators such as acetylcholine. with two of these having no overt sign of behavioral control during clinical assessment. 2001). 51. bilateral lesions in many of these nuclei cause a global loss of consciousness. These neuromodulators mediate the alternation between wakefulness and sleep. Lastly. while decreasing levels occur during non-REM or slowwave sleep. 2004). are associated with a selective loss of cholinergic neurons. Comparatively small (1 cm3 or less) bilateral lesions in the ILN can completely eliminate awareness (Bogen. They can widely influence the cortex through direct axonal projections (Fig. such as Parkinson’s disease. VII.

1096 51.3). It is implicitly assumed by most neurobiologists that the relevant variables giving rise to consciousness are to be found at the neuronal level. the observation that the quantum states of multiple objects. For example. 2010). BEHAVIORAL AND COGNITIVE NEUROSCIENCE . 51. rather than at the molecular level. Perturbing or inactivating the NCC for any one specific conscious experience will affect the percept or cause it to disappear. As defined by Crick and Koch (2003). the cerebellum is not part of the NCC. And even if quantum entanglement were to occur inside individual cells. 2000). One key objective has been to search for the neuronal correlates—and ultimately the causes—of consciousness. among the synaptic release or the action potentials in one or more population of cells. What characterizes the NCC? What are the communalities between the NCC for seeing and for hearing? Will the NCC involve all pyramidal neurons in cortex at any given point in time? Or only a subset of long-range pyramidal cells in frontal lobes that project to the sensory cortices in the back? Only layer 5 cortical cells? Neurons that fire in a rhythmic manner? Neurons that fire in a synchronous manner? These are some of the proposals that have been advanced over the years (Chalmers. Thus. yet a third one for hearing a siren. That is. Collini et al. That is. 2009). This definition of the NCC stresses the word “minimal” because the question of interest is which subcomponents of the brain are actually needed. The role of quantum mechanics for the photons received by the eye and for the molecules of life is not controversial.. 69 billion are in the cerebellum (Herculano-Houzel. and so on. While activity in some population of neurons may underpin a percept in one case. the neuronal correlates of consciousness (NCC) are the minimal neuronal mechanisms jointly sufficient for any one specific conscious percept (Fig. diffusion and action NCC Outside world Inside the brain FIGURE 51. by optogenetics or by cortical microstimulation—the subject would experience the associated percept. From Koch (2004). about four out of every five brain cells are small cerebellar granule neurons. a different population might mediate a related percept if the former population is lost or inactivated. another one for seeing grandmother. of the 86 billion neurons in the human brain. This definition does not focus on the necessary conditions for consciousness because of the great redundancy and parallelism found in neurobiological networks. and unsteady gait (Lemon & Edgley. violating our intuition about locality (entanglement is also the key feature of quantum mechanics exploited in quantum computers). VII. If the NCC could be induced artificially—for instance. may be highly correlated even though they are spatially separated. Yet the main deficits of people born without a cerebellum—a rare occurrence—or that lose part of the cerebellum to stroke or other trauma are ataxia. Every phenomenal. A few scholars have proposed that macroscopic quantum behaviors underlie consciousness. But there is no evidence that any components of the nervous system—a 37° Celsius wet and warm tissue strongly coupled to its environment—display quantum entanglement (although there is evidence for quantum coherence in photosynthetic proteins at room temperature. Of particular interest here is entanglement. 2010).3 Conscious percept The Neuronal Correlates of Consciousness (NCC) are the minimal set of neural events and structures—here synchronized action potentials in neocortical pyramidal neurons—sufficient for a specific conscious percept or memory. trains of spikes in granule cells—or their absence—do not contribute in any substantive way to conscious states. subjective state will have associated NCC: one for seeing a red patch. such as two coupled electrons. The vast majority of experiments concerned with the NCC refer to either electrophysiological recordings in monkeys or functional brain imaging data in humans. slurred speech. THE NEUROSCIENCE OF CONSCIOUSNESS THE NEURONAL CORRELATES OF CONSCIOUSNESS Progress in addressing the mind-body problem has come from focusing on empirically accessible questions rather than on eristic philosophical arguments with no clear resolution.

change blindness. in a high-level cortical area such as the inferior temporal (IT) cortex along the ventral pathway. For example. and the bottom row the monkey’s behavior. In a related perceptual phenomena. the percept associated with an image projected into one eye is suppressed by flashing another image into the other Firing rate (Hz) Input to two eyes 100 50 0 Pattern 0 Pattern 5 10 Face Pattern 15 Face Report 20 Time (sec) FIGURE 51. The cell responded only weakly to either the sunburst design or to its optical superposition with the image of a monkey’s face. permitting the footprints of visual consciousness to be tracked in the brain.4 A fraction of a minute in the life of a typical IT cell while a monkey experiences binocular rivalry. The distribution of the switching times and the way in which changing the contrast in one eye affects the reports leave little doubt that monkeys and humans experience the same basic phenomenon. The second row shows the individual spikes. In a series of elegant experiments. 2005). that can be precisely controlled. One example is the Necker cube that can be perceived in one of two different ways in depth. Here. one of these to each eye. THE NEURONAL BASIS OF PERCEPTUAL ILLUSIONS The possibility of precisely manipulating visual percepts in time and space has made vision a preferred modality for seeking the NCC. a small image—for example. inattentional blindness—in which the seemingly simple and unambiguous relationship between a physical stimulus in the world and its associated percept in the privacy of the subject’s mind is disrupted (Kim & Blake. In primary visual cortex (V1). with dotted vertical boundaries marking stimulus transitions.4). only a small fraction of cells weakly modulate their response as a function of the percept of the monkey. Despite the constant retinal stimulus. observers perceive the horizontal grating to alternate every few seconds with the vertical one. At the cellular level. VII. almost all neurons responded only to the perceptual dominant stimulus. Psychologists have perfected a number of techniques—masking. BEHAVIORAL AND COGNITIVE NEUROSCIENCE . binocular rivalry. to the stimulus that was being reported. 2002). 1998) recorded from a variety of visual cortical areas in the awake macaque monkey while the animal performed a binocular rivalry task. when a face and a more abstract design were presented. The upper row indicates the visual input to the two eyes. Logothetis and colleagues (Logothetis. a “face” cell fired only when the animal indicated by its performance that it saw the face and not the pattern presented to the other eye (Fig. Logothetis (private communication) as modified by Koch (2004). not seen. Another one. the third the smoothed firing rate. but not both. In contrast. In a perceptual illusion. the interaction of neurons is governed by classical physics (Koch & Hepp. the physical stimulus remains fixed. From N. The brain does not allow for the simultaneous perception of both images. The majority of cells responded to one or the other retinal stimulus with little regard to what the animal perceived at the time. a vertical grating—is shown to the corresponding location in the right eye. is binocular rivalry (Blake & Logothetis. Perception of the face was consistently accompanied (and preceded) by a strong increase in firing rate. the monkey’s perception vacillated back and forth between seeing the face (“Face”) and seeing the bursting sun (“Pattern”). This result implies that the NCC involves activity in neurons in inferior temporal cortex. With such techniques. Macaque monkeys can be trained to report whether they see the left or the right image. a horizontal grating—is presented to the left eye and another image—for example. that is. while the percept fluctuates. 51. 2010). The animal was taught to press a lever when it saw either one or the other image. motion-induced blindness. During binocular rivalry (gray zone).1097 THE NEURONAL BASIS OF PERCEPTUAL ILLUSIONS potential generation and propagation—the principal mechanism for getting information into and out of neurons—would destroy superposition. continuous flash suppression. In this manner the neural mechanisms that respond to the subjective percept rather than the retinal stimulus can be isolated. flash suppression. a stimulus can be perceptually suppressed for seconds or even minutes at a time: the image is projected into one of the observer’s eyes but it is invisible.

PERCEPTUAL PUZZLES OF CONTEMPORARY INTEREST The attributes of even simple percepts vary along a continuum. a rare form of visual migraine. Its methodological advantage over binocular rivalry is that the timing of the perceptual transition is determined by an external trigger rather than by an internal event. 1998). either heard or not. rather like the discrete frames in a movie (Purves. rather than gradually emerging from the noisy background? The perception of the world around us would then be a superposition of many elementary. 2010a). A number of compelling observations link perception with fMRI BOLD activity in human V1 and even LGN (Lee. without any movement in between. when the stimulus is present on the retina but is perceptually suppressed. Tsuchiya & Koch. For instance. BEHAVIORAL AND COGNITIVE NEUROSCIENCE . a patch of color has a brightness and a hue that are variable. However. even though legions of V1 neurons fire vigorously to the same stimulus (Sheinberg & Logothetis. They demonstrate quite conclusively that BOLD activity in the upper stages of the ventral pathway (e. Vaughan. binary percepts (Sergent & Dehaene. That is. 2006. & Koch. & Koch. 2008). 2007). its slant could be predicted on a single trial basis with better than chance odds from the V1 (but not from V2 or V3) BOLD signal. is it possible that each particular. 2006). yet no hole in the field of view is apparent.g. Stetson. For instance. 2005). The majority of responsive cells in inferior temporal cortex and in the superior temporal sulcus follow the monkey’s behavior—and therefore its percept. These data are at odds with single neuron recordings from the monkey. for a review of many of these experiments see van Boxtel. 2005. Is perception continuous. however. & Dehaene. Indeed. when the animal perceives a cell’s preferred stimulus. the neuron fires. A plausible explanation is that V1 neurons receive feedback signals during conscious perception that are not. consciously experienced. is V1 part of the NCC (Crick & Koch. even though the stimulus orientation was so efficiently masked that subjects performed at chance levels when trying to guess the orientation. There is a lively debate about the extent to which neurons in primary visual cortex simply encode the visual stimulus or are directly responsible for expressing the subject’s conscious percept. That is. it may not be perceived that way (Bartels & Zeki. While retinal neurons often correlate with visual experience. 1995)? It is clear that retinal neurons are not part of the NCC for visual experiences. 2003a). just as a simple tone has an associated loudness and pitch. & Andrews. THE NEUROSCIENCE OF CONSCIOUSNESS eye (while the original image remains). there are no photoreceptors at the blind spot.1098 51. is an old one. In cinematographic vision (Sacks. most often related to EEG rhythms in various frequency ranges (from theta to beta). percept is allor-none? Might a pure tone of a particular pitch and loudness be experienced as an atom of perception. like a river. & Heeger. 2002). although subjects did not give any behavioral indication that they saw the orientation of the stimulus. What all of these experiments demonstrate is that the neuronal basis of consciously experienced perceptions can be identified and studied using standard neuroscience tools. Paydarfar. or does it consist of a series of discontinuous batches. 2004). even though a change in the color of an object occurs simultaneous with a change in its direction of motion. 1996. What is the relationship between endogenous. the fusiform face area and the parahippocampal place area) follow the percept and not the retinal stimulus (Rees & Frith. Nakayama. & Eagleman. Haynes and Rees (2005) exploited multivariate decoding techniques to read out perceptually suppressed information (the orientation of a masked stimulus) from V1 BOLD activity. 2002. 1997). The hypothesis that visual perception is quantized in discrete batches of variable duration. it has been shown that attention can be allocated to a perceptually invisible stimulus (Naccache. That is. Cui. Tsuchiya. in dreams vivid imagery occurs despite closed eyes and so on). Blake. This finding supports the hypothesis that information present in V1 is not accessible to visual consciousness. & Kanwisher. A large number of fMRI experiments have exploited binocular rivalry and related illusions to identify the hemodynamic activity underlying visual consciousness in humans. Single neuron recordings in the medial temporal lobe of epileptic patients during flash suppression likewise demonstrate abolition of their responses when their preferred stimulus is present on the retina but not consciously seen by the patient (Kreiman. This question is receiving renewed “attention” due to the development of a powerful visual masking technique that can suppress stimuli for minutes at end (continuous flash suppression.. 2007). 2004). Tong. the cell falls silent. sufficient to drive the cells to spike (Maier et al. This idea is being revisited in light of the discrepancies of timing of perceptual events within and across different sensory modalities. VII. the subject sees the movement of objects as fractured in time. top-down attention and consciousness? Although these are frequently coextensive—subjects are usually conscious of what they attend to—there is considerable evidence that argues that these are distinct neurobiological processes (Koch & Tsuchiya. the spiking activity of retinal ganglion cells does not accord with visual experience (for example. as a succession of different configurations and positions. Montague. VanRullen & Koch. Blandin.. Fried.

2000. They are characterized by rapid and stereotyped sensory-motor actions called zombie behaviors (Koch & Crick. 2010b. Dehaene & Changeux. into V4. subjects can pay attention to something without seeing what they are paying attention to! In other experiments. The conscious mode for vision depends largely on the early visual areas (beyond V1) and especially on the ventral “what” stream. limb adjustments. The basis of this inference is clinical case studies and fMRI experiments in normal subjects (Corbetta & Shulman. 1977). This is the hypothesis at the heart of the global workspace model of consciousness (Baars. 2003b). 2001). It seems possible that visual zombie modes in the cortex mainly use the dorsal stream in the parietal region (Milner & Goodale. at least under some circumstances. Dehaene et al. Conscious perception requires more sustained. At this point. BOLD activity in the fusiform (visual) cortex and in a spatially extended network of midline prefrontal and inferior parietal cortices tracked conscious perception. Whether or not subjects see what they are looking at makes very little difference to the hemodynamic signal in V1. soccer. and even position of a single image flashed onto the retina of the fixating animal. Part of the habit system that controls automatic behavior (Shiffrin & Schneider. When exploring the neural basis of these processes. here distinguishing animal from nonanimal pictures. flashed 80–100 msec after onset of a first image. 1992). far too slow for conscious perception to be involved.5 msec and about 100 msec after image onset) the category. BEHAVIORAL AND COGNITIVE NEUROSCIENCE . in the absence of any conscious experience. and highly trained sensory-motor task—dribbling a soccer ball or typing on a keyboard—can interfere with its smooth execution.FORWARD VERSUS FEEDBACK PROJECTIONS That is. prefrontal. identity. something well known to athletes and their trainers. may be one of the principal functions of consciousness. & Lamme. and related structures that support short-term memory. until it affects motorneurons in the spinal cord that control the finger press (as in a typical laboratory experiment). reverberatory neural activity. Fize. Such feedback loops would explain why in backward masking a second stimulus. Whether the converse also occurs—being conscious of something without attending to it—remains an open question. planning. 51. can still interfere with (mask) the percept of the first image. 2011). Watanabe et al. allpurpose conscious mode that deals with more complex aspects of the sensory input (or a reflection of these. The conscious system may interfere somewhat with the concurrent zombie systems (Logan & Crump. with a limited behavioral repertoire. 2011). and other processes intimately related to consciousness. and DiCarlo (2005) were able to decode from the spiking activity of a couple of hundred neurons in monkey IT (over intervals as short as 12. 1995. The hypothesis that the basic processing of information is feedforward is supported most directly by the short times required for a selective response to appear in IT cells (Perrett et al. cluttered images) can be accomplished by cortex within 130–150 msec (Thorpe. such a feed-forward network implements a zombie behavior in the Koch and Crick (2001) sense—rapidly and efficiently subserving one task. transient. visual attention and consciousness—as assayed via stimulus visibility—in human primary visual cortex. the sustained neural activity rapidly propagates to parietal. as in imagery) and takes time to decide on appropriate responses. The reverberatory activity builds up over time until it exceeds a critical threshold. 2008). Such automatic behaviors are complemented by a nonhabit. claustrum. while attention strongly modulates the BOLD response. Fahrenfort. 1995). these behaviors can be thought of as cortical reflexes. and multimodality integration. it is therefore critical to not confound consciousness with attention. or any other athletic activity. Sensory information is processed in VII. most likely via global feedback from frontal regions of neocortex back to sensory cortical areas in the back (Crick & Koch. Poggio. 2009): focusing consciousness onto the smooth execution of a complex. driving a bicycle. thalamus.. and anterior cingulate cortical regions. However. executing well-rehearsed sequences in tennis. Kreiman. planning. speech. Lamme & Roelfsema. dissociate selective. and unconscious (Milner & Goodale. Examples include eye and hand movements. Coupled with a suitable motor output. Seemingly complex visual processing (such as detecting animals in natural. Scholte. 1996. It is plausible that such behaviors are mediated by a purely feed-forward moving wave of spiking activity that passes from the retina through V1. VanRullen & Koch. A consciousness mode is needed because otherwise a vast number of different zombie modes would be required to react to unusual events. & Marlot.5). FORWARD VERSUS FEEDBACK PROJECTIONS Many actions in response to sensory inputs are fast. visual attention has an opposing effect on afterimage duration than visual consciousness (van Boxtel. parietal activity can affect consciousness by producing attentional effects on the 1099 ventral stream. slower. IT and prefrontal cortex. rapid. Tsuchiya. This latter aspect. masked words with the activity evoked when the words were not masked (Fig. and so on. 2002). keyboard typing.. 1995). (2001) contrasted brain activity during presentation of flashed. Having both a zombie mode that responds in a well-rehearsed and stereotyped manner as well as a slower system that allows time for thinking and planning more complex behavior is a great evolutionary discovery. Hung. 1989. & Koch. Indeed.

data-driven approach will not lead to an understanding of why certain structures and processes have a privileged relationship with subjective experience. 2011). For example. it enters into a global neuronal workspace located in prefrontal cortical structures.. and of the neural correlates of nonconscious habit or zombie behaviors on the other. Competition inside the global neuronal workspace prevents more than one or a very small number of percepts to be simultaneously and actively represented. e. but of much different amplitude. 1 mm) sheet of neurons underneath the insular cortex.5 The Effect of Visual LION or Visible word or blank LION or Masked word or blank an array of feed-forward structures. and receives input from. or the World Wide Web as a whole. Both seen and masked words activated regions in the left ventral pathway. In summary. perhaps all cortical regions. will hopefully lead to a better understanding of what distinguishes neural structures or processes that are associated with consciousness from those that are not. it is not known to what extent animals whose nervous systems have an architecture considerably different from the mammalian neocortex are conscious. akin to a conductor of the cortical orchestra. whether artificial systems. The brain’s response to seen and unseen words. (2001). Yet such an opportunistic. parietal. This had a dramatic effect on the cortical fMRI response (the activity following the image sequences with words was compared to the sequences with blanks). it is surmised that consciousness requires sustained but well-organized neural activity dependent on integration across cortex. which behave with considerable intelligence. with what architecture. THE NEUROSCIENCE OF CONSCIOUSNESS Ti m e FIGURE 51. and above the putamen.g. buried in white matter structures. are or can become conscious (as widely assumed in science fiction. If it is powerful enough. remains speculative (Koch and Tononi. can possess conscious states. It is a thin (ca. AN INFORMATION-THEORETICAL THEORY OF CONSCIOUSNESS At present.1100 51. Progress in the study of the NCC on the one hand. No words were seen in the right stream. Crick and Koch (2005) surmised that the claustrum is critical to the integration of information underlying consciousness. This interpretation feeds back to the sensory representation in visual cortex. such as computers. why is it that neurons in corticothalamic circuits are essential for VII. robots. since each word was preceded and followed by a slide covered by random symbols. What is needed is a theory of consciousness that explains in quantitative terms what type of systems. Modified from Dehaene et al. Masking. Conscious perception triggered additional widespread activation in left parietal and prefrontal cortices. One hitherto neglected structure in this regard is the claustrum. while rapid but transient neural activity in the thalamo-cortical system can mediate complex behavior without conscious sensation. Volunteers looked at a stream of briefly flashed images. Furthermore. such as primary sensory cortices. It projects to. BEHAVIORAL AND COGNITIVE NEUROSCIENCE . and frontal lobes. by accessing memory and planning systems. perceptually obscuring the letters. From there it is widely broadcast by long-range cortico-cortical projections and placed into context—for instance. extending all the way into temporal. the paranoid computer HAL in the film 2001).

2008). In order to advance the resolution of these and similar questions. Φ can loosely be thought of as the representational capacity of the system (as in Fig. Thus. For example. 2008). 2003) is based on the differential requirement for awareness of trace versus delay associative eyeblink conditioning in humans (Clark & Squire. 1998). and delicate manner VII. by using simple computer simulations. Classically. Progress in understanding the circuitry of consciousness therefore demands a battery of behaviors (akin to but different from the well-known Turing test for intelligence) that the subject—a newborn infant. Massimini et al. it can be estimated. During slow-wave sleep. Conversely. the conscious experience of nouns independently of the verbs. 2008). when a subject consciously experiences reading this particular phrase.1101 CONCLUSION conscious experience. For example. Similarly. 2012). (2005) compared multichannel EEG of awake and conscious subjects in response to TMS pulses to the EEG when the same subjects were deeply asleep—a time during which consciousness is much reduced. ink colors. like the mammalian thalamocortical system. the initial response was stronger but was rapidly extinguished and did not propagate beyond the stimulation site. and a brief and intense magnetic field generates a weak electrical current in the gray matter underlying the skull. Φ is low for systems that are made up of small. 2008) and during loss of consciousness in patients (Rosanova et al. BEHAVIORAL AND COGNITIVE NEUROSCIENCE . how it can be measured. may be related. Hudetz. information associated with the occurrence of a conscious state is also integrated. The only promising candidate for such a theoretical framework is the information integration theory of consciousness (Tononi. It cannot be subdivided into components that are experienced independently. monkey. the reduction of uncertainty among alternatives constitutes information. and so on). despite levels of neural firing in the thalamocortical system that are comparable to the levels of firing in wakefulness? Information theory may be such a tool that establishes at the fundamental level what consciousness is. Although Φ is not easy to calculate exactly for realistic systems (Balduzzi & Tononi. immobilized patient. one particular mouse model of contingency awareness (Han et al. think of the same phrases spoken aloud. the theory claims that a physical system can generate consciousness to the extent that it integrates information. in all possible fonts. Furthermore.. the fading of consciousness during certain stages of sleep. whereas cerebellar neurons. it will be imperative to record from a large number of neurons simultaneously at many locations throughout the cortico-thalamo system and related satellites in people or behaving animals. or for networks of randomly or uniformly connected units. is obtained by determining the minimum repertoire of different states that can be produced in one part of the system by perturbations of its other parts (Tononi. Any one experience is an indivisible whole. 1998). to the breakdown of information integration among specialized thalamocortical modules. the theory introduces a measure of a system’s capacity to integrate information. This requires that the system has a large repertoire of available states (information) that cannot be decomposed into a collection of causally independent subsystems (integration). it is possible to show that Φ is high for neural architectures that conjoin functional specialization with functional integration. like the cerebellum. This measure. an initial response at the stimulation site was followed by a sequence of waves that moved to connected cortical areas several centimeters away. called Φ. every experience represents one particular conscious state out of a huge repertoire of possible conscious states. Yet many aspects of this ancient set of questions now fall squarely within the domain of science. visual shapes cannot be experienced independently of their color. such as monkeys or mice. The notion that consciousness has to do with the brain’s ability to integrate information has been tested directly by transcranial magnetic stimulation (TMS). her. Tononi & Edelman. Again. The growing ability of neuroscientists to manipulate in a reversible. transient. and sizes. it has been the domain of armchair speculations and esoteric debates with no apparent resolution. A coil is placed above the skull. CONCLUSION Ever since the Greeks first considered the mind-body problem more than two millennia ago. quasi-independent modules. as predicted by the theory. despite their huge numbers. Thus. & Tononi. Importantly. as well as during anesthesia (Alkire. say. This is not an insurmountable step for mammals such as the monkey or the mouse that share many behaviors and brain structures with humans. 1996.1). Any one particular conscious state rules out a huge number of alternative experiences. by contrast. and what requisites a physical system must satisfy in order to generate it (Chalmers. are not? And what is wrong with cortical zombie systems that make them unsuitable to yield subjective experience? Or why is it that consciousness wanes during slow-wave sleep early in the night. nor can the left half of the visual field of view be experienced independently of the right half. the conscious experience of this particular phrase cannot be experienced as subdivided into.. 51. Based on these two considerations. a huge number of other possible experiences are ruled out (consider all possible written phrases that could have been written in this space. deliberate. It posits that consciousness is extraordinarily informative. or read and spoken. During quiet wakefulness. or it to possess some measure of conscious perception. Thus. or mouse—has to pass before considering him.

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