Neural correlates of consciousness
The Neural Correlates of Consciousness (NCC) can be defined as the minimal neuronal mechanisms jointly sufficient for any one specific conscious percept (Crick & Koch 1990).
The Neurobiological Approach to Consciousness
Consciousness is a puzzling, state-dependent property of certain types of complex, biological, adaptive, and highly interconnected systems. A science of consciousness must strive to explain the exact relationship between phenomenal, mental states and brain states. This is the heart of the classical mind-body problem: What is the nature of the relationship between the immaterial, conscious mind and its physical basis in the electrochemical interactions in the body? Brain scientists are exploiting a number of empirical approaches to shed light on the neural basis of consciousness. This article reviews these approaches and summarizes what has been learnt. See http://www.klab.caltech.edu/~koch/glossary.html for a glossary of related terms.
The Neural Correlates of Consciousness
Progress in addressing the mind-body problem has come from focusing on empirically accessible questions rather than on eristic philosophical arguments. Key is the search for the neuronal correlates -- and ultimately the causes -- of consciousness.
The above definition of Neural Correlates of Consciousness stresses the attribute minimal because the entire brain is clearly sufficient to give rise to consciousness. The question of interest is which of its subcomponents are essential to produce a conscious experience (Figure 1). For instance, it is likely that neural activity in the cerebellum does not underlie any conscious perception, and thus is not part of the Neural Correlates of Consciousness. That is, trains of spikes in Purkinje cells (or their absence) will not induce a sensory percept although they may ultimately affect some behaviors (such as eye movements).
This definition does not focus exclusively on the necessary conditions because of the great redundancy and parallelism found in neurobiological networks. While activity in some population of neurons may underpin a percept in one case, a different population might mediate a related percept if the former population is lost or inactivated.
Every phenomenal, subjective state will have associated Neural Correlates of Consciousness: one for seeing a red patch, another one for seeing grandmother, yet a third one for hearing a siren, etc. Perturbing or inactivating the Neural Correlates of Consciousness for any one specific conscious experience will affect the percept or cause it to disappear. If the Neural Correlates of Consciousness could be induced artificially, for instance by cortical microstimulation in a prosthetic device or during neurosurgery, the subject would experience the associated percept.
What characterizes the Neural Correlates of Consciousness? What are the communalities between the Neural Correlates of Consciousness for seeing and for hearing? Will the Neural Correlates of Consciousness involve all pyramidal neurons in cortex at any given point in time? Or only a subset of long-range projection cells in frontal lobes that project to the sensory cortices in the back? 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 2000).
It should be noted that discovering and characterizing the Neural Correlates of Consciousness in brains is not the same as a theory of consciousness. Only the latter can tell us why particular systems can experience anything, why they are conscious, and why other systems - such as the enteric nervous system or the immune system - are not. However, understanding the Neural Correlates of Consciousness is a necessary step toward such a theory.
Level of Arousal and Content of Consciousness
States of Consciousness and Conscious States
There are two common, but quite distinct, usages of the term consciousness, one revolving around arousal and states of consciousness and another one around the content of consciousness and conscious states.
To be conscious of anything, the brain must be in a relatively high state of arousal (sometimes also referred to as vigilance). This is as true of wakefulness as it is of REM sleep that is vividly, consciously experienced in dreams, although usually not remembered. The level of brain arousal, measured by electrical or metabolic brain activity, fluctuates in a circadian manner and is influenced by lack of sleep, drugs and alcohol, physical exertion, etc. in a predictable manner. High arousal states are usually associated with some conscious state – a percept, thought or memory - that has a specific content. We see a face, hear music, remember an incident, plan an experiment, or fantasize about sex. Indeed, it is unlikely that one can be awake without being conscious of something. Referring to such conscious states is conceptually quite distinct from referring to states of consciousness that fluctuate with different levels of arousal. Arousal can be measured behaviorally by the signal amplitude that triggers some criterion reaction (for instance, the sound level necessary to evoke an eye movement or a head turn toward the sound source). Clinicians use scoring systems such as the Glasgow Coma Scale to assess the level of arousal in patients.
Different levels or states of consciousness are associated with different kinds of conscious experiences. The awake state in a normal functioning individual is quite different from the dreaming state (for instance, the latter has little or no self-reflection) or from the state of deep sleep. In all three cases, the basic physiology of the brain is changed, affecting the space of possible conscious experiences. Physiology is also different in altered states of consciousness, for instance after taking psychedelic drugs when events often have a stronger emotional connotation than in normal life. Yet another state of consciousness has been reported to occur during certain meditative practices, when conscious perception and insight are assumed to be enhanced compared to the normal waking state.
In some obvious but difficult to rigorously define manner, the richness of conscious experience increases as an individual transitions from deep sleep to drowsiness to full wakefulness. 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.g., the integrated-information-theoretical account of consciousness; see Tononi 2004). Inactivating all of visual cortex in an otherwise normal individual would significantly reduce the dimensionality of conscious experience since no color, shape, motion, texture or depth could be perceived. As behavioral arousal increases, so does the range and complexity of behaviors that an individual is capable of. 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, and the person is difficult to wake up. Yet this low level of behavioral arousal goes, paradoxically, hand in hand with high metabolic and electrical brain activity and conscious, vivid states.
These observations suggest a two-dimensional graph (Figure 2) in which the richness of conscious experience (its representational capacity) is plotted as a function of levels of behavioral arousal or responsiveness.
Global Disorders of Consciousness
Global disorders of consciousness can likewise be mapped onto this plane (Figure 2). Clinicians talk about impaired states of consciousness as in “the comatose state”, “the persistent vegetative state” (PVS), and “the minimally conscious state” (MCS). Here, "state" refers to different levels of consciousness, from a total absence in coma, PVS and general anesthesia, to a fluctuating and limited form of conscious sensation in MCS, sleep walking or during a complex partial epileptic seizure (Schiff 2004).
The repertoire of distinct conscious states or experiences that are accessible to a patient in MCS is presumably minimal (mainly pain and discomfort, possibly sporadic sensory percepts), immeasurably smaller than the possible conscious states that can be experienced by a healthy brain. In the limit of brain death, the origin of this space has been reached with no experience at all (Figure 2). A more desirable state is global anesthesia during which the patient should not experience anything – to avoid psychological trauma – but the level of arousal during the operation should be compatible with clinical exigencies. While anesthetics may, in principle, be useful for the study of consciousness, they have as yet failed to provide breakthrough insights about the Neural Correlates of Consciousness. This is mainly due their diverse mechanisms of molecular action, targeting receptors throughout large parts of the brain. As our ability increases to differentiate subreceptor variation and target them with molecular tools by means of genetic in vivo studies (Rudolph & Antkowiak 2004), this is likely to change.
Given the absence of any accepted theory for the minimal neuronal criteria necessary for consciousness, the distinction between a PVS patient – who shows regular sleep-wave transitions and who may be able to move their eyes or limbs or smile in a reflexive manner as in the case of Terri Schiavo in Florida - and a MCS patient who can communicate (on occasion) in a meaningful manner (for instance, by differential eye movements) and who shows some signs of consciousness, is often difficult in a clinical setting. Functional brain imaging may prove immensely useful here.
Blood-oxygen-level-dependent functional magnetic resonance imaging (BOLD fMRI) recently demonstrated that a patient in a vegetative state following a severe traumatic brain injury showed the same pattern of brain activity as normals when asked to imagine playing tennis or to imagine visiting all rooms in her house (Owen et al. 2006). Differential brain imaging of patients with such global disturbances of consciousness (including akinetic mutism) reveal that dysfunction in a widespread cortical network including medial and lateral prefrontal and parietal associative areas is associated with a global loss of consciousness (Laureys 2005). Impaired consciousness in epileptic seizures of the temporal lobe was likewise found to be accompanied by a decrease in cerebral blood flow in frontal and parietal association cortex and an increase in midline structures such as the mediodorsal thalamus (Blumenfeld et al. 2004).
Localized Brain Lesions affecting Consciousness
In contrast to diffuse cortical damage, relatively discrete bilateral injuries to midline (paramedian) subcortical structures can also cause a complete loss of consciousness. 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 form of consciousness to occur. One such example is the heterogeneous collection of more than two dozen (on each side) of nuclei in the upper brainstem (pons, midbrain and in the posterior hypothalamus) collectively referred to as the reticular activating system (RAS). These nuclei – three-dimensional collections of neurons with their own cytoarchitecture and neurochemical identity - release distinct neuromodulators such as acetylcholine, noradrenaline/norepinephrine, serotonin, histamine and orexin/hypocretin. Their axons project widely throughout the brain (Figure 3). These neuromodulators control the excitability of thalamus and forebrain and mediate the alternation between wakefulness and sleep as well as the general level of both behavioral and brain arousal. Acute lesions of nuclei in the RAS can result in loss of consciousness and coma. However, eventually the excitability of thalamus and forebrain can recover and consciousness can return (Villablanca 2004). Another enabling factor for consciousness are the five or more intralaminar nuclei (ILN) of the thalamus. These receive input from many brainstem nuclei and project strongly to the basal ganglia and, in a more distributed manner, into layer I of much of neocortex. Comparatively small (1 cm3 or less), bilateral lesions in the thalamic ILN completely knock out all awareness (Bogen 1995).
In summary, a plethora of nuclei with distinct chemical signatures in the thalamus, midbrain and pons must function for a subject to be in a sufficient state of brain arousal to experience anything at all. These nuclei belong to the enabling factors for consciousness. Conversely, it is likely that the specific content of any one conscious sensation is mediated by neurons in cortex and their associated satellite structures, including the amygdala, thalamus, claustrum and the basal ganglia.
The brain has a remarkable degree of bilateral symmetry. The mind, however, has but a single stream of consciousness, not two. Under ordinary conditions, the two hundred million fibers making up the corpus callosum, together with the anterior commissure and other minor bundles, integrate neural activity in the two halves of the forebrain such that only a single, integrated percept arises.
In certain cases of intractable epileptic seizures, part or all of the corpus callosum are surgically cut. Remarkably, after recovery, these patients usually act, speak, and feel no differently from before. They do not complain of a loss of half their visual field or of other dramatic deficits. Upon closer inspection, however, a persistent and profound disconnection (split-brain) syndrome can be observed. If specific sensory information is provided to one or the other hemisphere, the information is not shared with its twin. A split-brain patient with typical (left hemispheric) language dominance is unable to name an image of an object presented in the left visual hemifield, but can pick this object from a group of objects using his left hand. This procedure involves conscious perception followed by a targeted motor response with the neural correlates necessarily being constrained to one hemisphere.
The primary conclusion from split-brain patients, work for which Roger Sperry was awarded the Nobel prize in 1981, is that both hemispheres are independently capable of conscious experience (Bogen 1993; Gazzaniga 1995). Whatever the neuronal correlates of consciousness, these must exist independently in both cortical hemispheres.
Another example of a complex impairment of conscious perception, not to be confused with the split-brain syndrome, is the neglect syndrome, properly called visuospatial hemineglect. It can be found after extensive damage typically to the right brain hemisphere affecting the inferior parietal cortex. Patients with a hemineglect syndrome show an impaired awareness of their left visual hemifield despite the visual pathway being completely intact.
The Neuronal Basis of Conscious Perception
The possibility of precisely manipulating visual percepts in time and space has made vision a preferred modality in the quest for the Neural Correlates of Consciousness. Psychologists have perfected a number of techniques – masking, binocular rivalry, continuous flash suppression, motion-induced blindness, change blindness, 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 and Blake 2004). In particular, 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 is invisible, not seen. In this manner the neural mechanisms that respond to the subjective percept rather than the physical stimulus can be isolated, permitting the footprints of visual consciousness to be tracked in the brain. In a perceptual illusion, the physical stimulus remains fixed while the percept fluctuates. The best known example is the Necker cube whose 12 lines can be perceived in one of two different ways in depth (Figure 4).
A perceptual illusion that can be precisely controlled is binocular rivalry. Here, a small image, e.g., a horizontal grating, is presented to the left eye, and another image, e.g., a vertical grating, is shown to the corresponding location in the right eye. In spite of the constant visual stimulus, observers consciously see the horizontal grating alternate every few seconds with the vertical one. The brain does not allow for the simultaneous perception of both images. Macaque monkeys can be trained to report whether they see the left or the right image. The distribution of the switching times and the way in which changing the contrast in one eye affects these leaves little doubt that monkeys and humans experience the same basic phenomenon. In a series of elegant experiments, Logothetis and colleagues (Logothetis 1998) recorded from a variety of visual cortical areas in the awake macaque monkey while the animal performed a binocular rivalry task. In primary visual cortex (V1), only a small fraction of cells weakly modulate their response as a function of the percept of the monkey. The majority of cells responded to one or the other retinal stimulus with little regard to what the animal perceived at the time. Conversely, in a high-level cortical area such as the inferior temporal (IT) cortex along the ventral (“what?”) pathway, almost all neurons responded only to the perceptually dominant stimulus (in other words, a “face" cell only fired when the animal indicated by its performance that it saw the face and not the pattern presented to the other eye; see Figure 5), implying that the Neural Correlates of Consciousness involves activity in neurons in inferior temporal cortex. However, it is likely that specific reciprocal interactions between IT cells and neurons in parts of the prefrontal cortex are necessary in order for the Neural Correlates of Consciousness to be generated.
In a related perceptual phenomenon, flash suppression, the percept associated with an image projected into one eye is suppressed by flashing another image into the other eye (while the original image remains). 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. The majority of cells in IT cortex and in the superior temporal sulcus of monkeys trained to report their percept during flash suppression follow the animal’s percept. That is, when the cell’s preferred stimulus is perceived, the cell responds. If the picture is still present on the retina but is perceptually suppressed, the cell falls silent, even though legions of primary visual cortex neurons fire vigorously to this stimulus (Leopold and Logothetis 1996; Sheinberg and Logothetis 1997). Single neuron recordings in the medial temporal lobe of epilepsy patients during flash suppression likewise demonstrate abolishment of their responses when their preferred stimulus is present but perceptually masked (Kreiman et al. 2002).
A number of fMRI experiments have exploited binocular rivalry and related illusions to identify the hemodynamic activity underlying visual consciousness in humans. They demonstrate quite conclusively that BOLD activity in the upper stages of the ventral pathway (e.g., the fusiform face area and the parahippocampal place area) as well as in early regions, including V1 and the lateral geniculate nucleus (LGN), follow the percept and not simply the retinal stimulus (Rees and Frith 2007). Furthermore, a number of elegant fMRI experiments (Haynes and Rees 2005; Lee et al., 2007) support the hypothesis that V1 is necessary, but not sufficient for visual consciousness (Crick and Koch 1995).
Forward versus Feedback Projections
Many actions in response to sensory inputs are rapid, transient, stereotyped, and unconscious (Milner and Goodale, 1995). They could be thought of as cortical reflexes and are characterized by rapid and somewhat stereotyped responses that can take the form of rather complex automated behavior as seen, e.g., in complex partial epileptic seizures. These automated responses, sometimes called zombie behaviors (Koch and Crick 2001), could be contrasted by a slower, all-purpose conscious mode that deals more slowly with broader, less stereotyped aspects of the sensory inputs (or a reflection of these, as in imagery) and takes time to decide on appropriate thoughts and responses. Without such a consciousness mode, a vast number of different zombie modes would be required to react to unusual events.
A feature that distinguishes humans from most animals is that we are not born with an extensive repertoire of behavioral programs that would enable us to survive on our own ("physiological prematurity"). To compensate for this, we have an unmatched ability to learn, i.e., to consciously acquire such programs by imitation or exploration. Once consciously acquired and sufficiently exercised, these programs can become automated to the extent that their execution happens beyond the realms of our awareness. Take as an example the incredible fine motor skills exerted in playing a Beethoven piano sonata or the sensorimotor coordination required to ride a motorcycle along a curvy mountain road. Such complex behaviors are possible only because a sufficient number of the subprograms involved can be executed with minimal or even suspended conscious control. In fact, the conscious system may actually interfere somewhat with these automated programs (Beilock et al. 2002).
From an evolutionary standpoint it clearly makes sense to have both automated behavioral programs that can be executed rapidly in a stereotyped and automated manner, and a slightly slower system that allows time for thinking and planning more complex behavior. This latter aspect may be one of the principal functions of consciousness.
It seems possible that visual zombie modes in the cortex mainly use the dorsal (“where?”) stream in the parietal region (Milner and Goodale, 1995). However, parietal activity can affect consciousness by producing attentional effects on the ventral stream, at least under some circumstances. The conscious mode for vision depends largely on the early visual areas (beyond V1) and especially on the ventral stream.
Seemingly complex visual processing (such as detecting animals in natural, cluttered scenes; see Fast Visual Processing) can be accomplished by the human cortex within 130-150 ms (Thorpe et al. 1996, VanRullen and Koch 2003), much too fast for eye movements and conscious perception to occur. Furthermore, reflexes such as the oculovestibular reflex take place at even more rapid time-scales. It is quite plausible that such behaviors are mediated by a purely feed-forward moving wave of spiking activity that passes from the retina through V1, into V4, IT and prefrontal cortex, until it affects motorneurons in the spinal cord that control the finger press (as in a typical laboratory experiment). The hypothesis that the basic processing of information is feedforward is supported most directly by the short times (approx. 100 ms) required for a selective response to appear in IT cells.
Conversely, conscious perception is believed to require more sustained, reverberatory neural activity, most likely via global feedback from frontal regions of neocortex back to sensory cortical areas (Crick and Koch, 1995) that builds up over time until it exceeds a critical threshold. At this point, the sustained neural activity rapidly propagates to parietal, prefrontal and anterior cingulate cortical regions, thalamus, claustrum and related structures that support short-term memory, multi-modality integration, planning, speech, and other processes intimately related to consciousness. Competition prevents more than one or a very small number of percepts to be simultaneously and actively represented. This is the core hypothesis of the global workspace model of consciousness (Baars 1988, Dehaene et al. 2003).
In brief, while rapid but transient neural activity in the thalamo-cortical system can mediate complex behavior without conscious sensation, it is surmised that consciousness requires sustained but well-organized neural activity dependent on long-range cortico-cortical feedback.
Other Aspects of Consciousness
Quantum Mechanics and Consciousness
It is implicitly assumed by most neurobiologists that the relevant variables giving rise to consciousness are to be found at the neuronal level, among the synaptic release or the action potentials in one or more population of cells, rather than at the molecular level.
A few scholars have proposed that macroscopic quantum behaviors underlie consciousness. Of particular interest here is entanglement, the observation that the quantum states of multiple objects, such as two coupled electrons, may be highly correlated even though they are spatially separated, violating our intuition about locality (entanglement is also the key feature of quantum mechanics hoped to be exploited in quantum computers). The role of quantum mechanics for the photons received by the eye and for the molecules of life is undisputed. But there is no evidence that any components of the nervous system - a 37o Celsius warm and wet tissue strongly coupled to its environment - display quantum entanglement. And even if quantum entanglement were to occur inside individual cells, diffusion and action potential generation and propagation, the principal mechanism for getting information into and out of neurons, would destroy superposition. At the cellular level, the interaction of neurons is governed by classical physics (Koch and Hepp 2006).
Volition and Consciousness
A particular aspect of the mind-body problem is the question of free will. The spectrum of views ranges from the traditional and deeply embedded belief that we are free, autonomous, and conscious actors to the view that we are biological machines driven by needs and desires beyond conscious access and without willful control. Whether volition is illusory or is free in some libertarian sense does not answer the question of how subjective states relate to brain states. The perception of free will, what psychologists call the feeling of agency or authorship (e.g. “I decided to lift my finger”), is certainly a subjective state with an associated phenomenal content (quale) no different in kind from the quale of a toothache or seeing marine blue. So even if free will is a complete chimera, the subjective feeling of willing an action must have some neuronal correlate.
Direct electrical brain stimulation during neurosurgery (Fried et al. 1991) as well as fMRI experiments implicate medial pre-motor and anterior cingulate cortices in generating the subjective feeling of triggering an action (Lau et al. 2004). In other words, the neural correlate for the feeling of apparent causation involves activity in these cortical regions.
Progress in the study of the Neural Correlates of Consciousness on one hand, and of the neural correlates of non-conscious behaviors on the other, will hopefully lead to a better understanding of what distinguishes neural structures or processes that are associated with consciousness from those that are not.
The growing ability of neuroscientists to manipulate in a reversible, transient, deliberate and delicate manner identified populations of neurons using methods from molecular biology in combination with optical tools (e.g., Adamantidis et al. 2007) opens the possibility of moving from correlation - observing that a particular conscious state is associated with some neural or hemodynamic activity - to causation. Exploiting these increasingly powerful tools depends on the simultaneous development of appropriate behavioral assays and model organisms amenable to large-scale genomic analysis and manipulation.
It is the combination of such fine-grained neuronal analysis in animals with ever more sensitive psychophysical and brain imaging techniques in humans, complemented by the development of a robust theoretical predictive framework and coupled to a more refined philosophical analysis, that will hopefully lead to a rational understanding of consciousness, one of the central mysteries of life.
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