Consciousness Poses Fundamental Problems for a Biological Theory of Mind
Exploration of the nature of spatial neglect and free will touches on one of the great issues of cognitive neural science, and in fact of all science: the nature of consciousness. The unique character of consciousness has attracted fierce interest and debate among philosophers of mind because it is difficult to see how consciousness might be explained in reductionist physical terms.
At the beginning of this book we stated that what we commonly call mind is a set of operations carried out by the brain. Because consciousness is a fundamental property of mind, it too must be a function of the brain and in principle we should be able to identify neural circuits that give rise to it. However, before we can develop theories of consciousness that can be tested by empirical science, we must first define consciousness in operational terms.
Here we should emphasize that, in general, the concepts that neuroscientists initially use to describe mental processes—such as learning, memory, or consciousness—are those developed by philosophers. Such concepts were formed without knowledge of how mental processes are mediated by the brain. Once neuroscientists define a specific mental process in psychological terms—and we can now do so quite precisely—they then can attempt to localize and analyze the neuronal systems that mediate the process. This approach, as we shall see, can now even be applied to consciousness.
Consciousness is ordinarily thought of as a state of self-awareness. Philosophers of mind such as John Searle and Thomas Nagel have defined three essential features of self-awareness: subjectivity, unity, and intentionality.
The subjectivity of self-awareness is the characteristic that poses the greatest philosophical and scientific challenge. Each of us has an awareness of a self that is the center of experience. Each of us experiences a world of sensations that feel unique and private. Our own experience seems much more real to us than the experiences of others. Our own ideas, moods, and sensations—our successes and disappointments, joys and pains—are experienced directly, whereas we can only indirectly appreciate other people's ideas, moods, and sensations. Is the aroma of lavender that I smell identical to your experience of lavender? This is not simply a question of our sensory capability. Even when sensory capabilities are measurably identical, the aroma of lavender is not only determined by the lavender but also by our personal history—the experience we recall from memory—and since experiential history is highly individualized, lavender may not produce the same subjective sensation in each of us.
Once we know how the aroma of lavender is mediated by neural signals that announce the presence of chemical molecules, how does our sensation, the conscious awareness of an aroma, arise from other neural networks of the brain?
The fact that conscious experience is fundamentally subjective raises the question of whether it is even possible to determine objectively some characteristics of consciousness that transcend individual experience. If the senses produce only subjective experience, the argument goes, those same senses cannot be the means of arriving at an objective understanding of experience.
The unity of self-awareness refers to the fact that our experience of the world at any given moment is felt as a single unified experience. All of the various sensory modalities are blended into a single experience. When we sit down to dinner we experience the chair against our back, the sound of music, and the fruity flavor of the wine as connected and simultaneous. When we speak to our dinner partners we do so in whole sentences; we are aware that we are completing an idea but pay little if any attention to the process of constructing sentences.
Finally, self-awareness has intentionality. That is, our conscious experience connects successive moments and we have the sense that successive moments are directed to some goal.
In earlier times these features of consciousness led some philosophers to a dualistic view of mind, a view that the body and the mind are very different substances—the body being physical and the mind existing in some nonphysical, spiritual medium. Today almost all philosophers of mind agree that what we call consciousness derives from physical properties of the brain. Thinkers about consciousness fall into two groups. The first group, of which Daniel Dennett is the most prominent advocate, thinks there is no problem of consciousness. Consciousness emerges quite simply from an understanding of neuronal activity. Dennett argues, much as did the neurologist John Hughlings Jackson a century earlier, that consciousness is not a discrete operation of the brain but the outcome of the computational activity of the association areas of the brain. The second group, which includes Francis Crick, Christof Koch, John Searle, Thomas Nagel, Antonio Damasio, and Gerald Edelman, believes that consciousness is a discrete phenomenon and that the issues of subjectivity, unity, and intentionality must be confronted if we are to understand how our experience is constructed.
Because consciousness has properties that other mental functions do not, a biological explanation poses a formidable problem, a problem so inherently difficult that the philosopher Colin McGinn has argued that consciousness is simply inaccessible to empirical study because of limitations inherent in human intelligence. Just as monkeys cannot understand quantum theory, humans cannot understand consciousness, McGinn argues. Conversely, Searle and Nagel argue that consciousness is accessible to analysis but we have been unable to explain it because it is a highly subjective and complex property of the brain unlike any function of the brain we understand—indeed, unlike any other subject of scientific inquiry.
Of the three features of consciousness, subjectivity is the most difficult to analyze empirically. Nagel and Searle illustrate the precise difficulty in the following way. Assume we succeed in studying a person's consciousness by recording the electrical activity of neurons in a region known to be important for consciousness while that person carries out a particular task requiring conscious attention. How do we then analyze the results? Can we say that the firing of a group of neurons causes a private subjective experience? Does a burst of action potentials in the thalamus and somatic sensory cortex switch information into consciousness so that a person now perceives an object in his hand and perceives it as round or square, hard or malleable? What empirical grounds do we have for believing that when a mother looks at her infant child the firing of cells in the inferotemporal cortex concerned with face recognition causes conscious recognition of her child's face?
As yet we do not know even in the simplest case how the firing of specific neurons leads to conscious perception. In fact, Searle argues that we lack even an adequate theoretical model of how an ontologically objective phenomenon—electrical signals in another person's brain—can cause an ontologically subjective experience such as pain. Because consciousness is irreducibly subjective, it lies beyond the reach of science as we currently practice it.
Similarly, Nagel argues that because current science is essentially a reductionist approach to understanding phenomena it cannot address consciousness without a significant change in method, one in which the elements of subjective experience are defined. These elements are likely to be basic components of brain function much as atoms and molecules are basic components of matter. According to Nagel, object-to-object reductions are not problematic because we understand, at least in principle, how the properties of a given type of matter arise from the molecules of which it is made. What we lack are rules for extrapolating subjective experience from the physicochemical properties of interconnected nerve cells.
Nagel argues that our complete lack of insight into the elements of subjective experience should not prevent us from discovering rules that relate conscious phenomena to cellular processes in the brain. In fact, Nagel believes that the knowledge needed to think about a more fundamental type of analytical reduction—from something subjective (experience) to something objective (physical)—can be gained only through the accumulation of cell-biological information. Only after we have developed a theory of mind that supports this novel and fundamental reduction will the limitations of the current reductionism become apparent. The discovery of the elementary components of subjective consciousness, Nagel argues, may require a revolution in biology and most likely a complete transformation of scientific thought.
Neurobiological Research on Cognitive Processes Does Not Depend on a Specific Theory of Consciousness
Most neural scientists whose work touches on the question of consciousness are not necessarily working toward or anticipating a revolution in scientific thought. Although neural scientists working on issues such as sensory perception and cognition must struggle with the difficulties of defining consciousness experimentally, these difficulties do not appear to preclude productive research. The physicist Steven Weinberg perhaps best expressed this attitude:
I don't see how anyone but George will ever know how it feels to be George. On the other hand, I can readily believe that at least in principle we will be able to explain all of George's behavior reductively, including what he says about what he feels, and that consciousness will be one of the emergent higher-level concepts appearing in this equation.
Indeed, neural science has made considerable progress in understanding the neurobiology of sensory perception without having to account for individual experience. Understanding the neural basis of perception of color and form, for example, does not depend on resolving the question of whether each of us sees the same blue. Despite the fact that perception of an object is constructed by the brain from piecemeal sensory information, and despite individual differences caused by experience, perception of an object is not arbitrary and appears to correspond to objective physical properties of the object. What we do not understand is the step from action potentials to awareness of an object.
Although the subjectivity of consciousness makes the neurobiological study of consciousness especially difficult, in principle such a study may not be insurmountable using current methods. The subjective nature of perception does not prevent one person from objectively studying what another person perceives. We have been able to correlate some regularities of perception with specific patterns of neuronal activity in different individuals under a variety of circumstances. The correlation between a neural event and a mental event, based on rigorous criteria, should be a sufficient first approximation of the neural process mediating a mental operation by any reasonable standards of scientific explanation. For this reason Crick and Koch emphasized that the first step in the analysis of consciousness is to find the neural correlates of consciousness, the minimal set of neural events that give rise to a conscious percept.
Finding the neural systems that mediate con sciousness may not be simple. Gerald Edelman and Stanislas Dehaene have argued that the neural correlates of consciousness are unlikely to be localized but rather widely distributed throughout the cerebral cortex and thalamus. There is extensive evidence of massive feedforward broadcasting as well as, feedback or recursive connections between cortical areas, which Dehaene believes may be essential for the conversion of unconscious to conscious perception.
By contrast, Crick and Koch believed that the most elementary neural correlates of consciousness are likely to involve only a small set of neurons, and therefore one should be able to determine the neural circuits to which they belong. Crick and Koch proposed a search for the neural activity that produces specific instances of consciousness, such as perception of the movement of an object, its shape, and its color. Having done that we may eventually be in a position to meet Searle's and Nagel's higher demands: to develop a theory of the correlations we discover empirically, to state the laws of correlation between neural phenomena and subjective experience.
Because at any moment we can be conscious of one of a large variety of sounds, smells, and objects as well as actions, consciousness must involve modulatory control over a variety of neural systems. Thus consciousness is required for many aspects of mental activity: visual perception, thinking, emotion, action, and the perception of self. Because we understand the visual system best, Crick and Koch argued that our efforts should be focused on visual perception and in particular on two phenomena: binocular rivalry and selective attention.
Studies of Binocular Rivalry Have Identified Circuits That May Switch Unconscious to Conscious Visual Perception
When two different images are presented simultaneously to the two eyes—horizontal bars to one eye, vertical bars to the other—the subject's perception alternates spontaneously from one monocular view to the other. Erik Lumer and his colleagues found in functional imaging experiments that whenever an individual switches from one eye to the next—from one conscious percept to the next—three sets of cortical areas are recruited. One is the ventral visual pathway of the temporal lobe, which is concerned with perceptions of objects and people. The others are the parietal and frontal regions, which are known to be involved in visual attention to space. Lumer and his colleagues suggest that the frontal and parietal areas are critical for conscious perception and that these areas focus awareness on specific internal representations of visual images.
Nikos Logothetis has carried out similar analyses at the level of individual neurons and confirmed that the competition between rivalrous stimuli in the two halves of the visual field is resolved late in the ventral pathway, in the inferior temporal cortex and the lower layers of the superior temporal sulcus. These regions in turn project to and receive connections from the prefrontal cortex. In light of these findings Crick and Koch argued that the pathways for conscious visual perception course through the inferior temporal cortex to the prefrontal and parietal cortices.
Selective Attention to Visual Stimuli Can Be Studied on the Cellular Level in Nonhuman Primates
Selective attention in vision is another useful starting point for a cell-biological approach to the study of consciousness. At any given moment we are aware of only a small fraction of the sensory stimuli that impinge on us. As we look out on the world, we focus on specific objects or scenes that have particular interest and exclude others.
If you raise your eyes from this book to look at a person entering the room, you are no longer attending to the words on this page. Nor are you attending to the decor of the room or other people in the room. This focusing of the sensory apparatus is an essential feature of all sensory processing, as Williams James first noted in his Principles of Psychology (1890):
Millions of items … are present to my senses which never properly enter my experience. Why? Because they have no interest for me. My experience is what I agree to attend to…. Everyone knows what attention is. It is the taking possession by the mind, in clear and vivid form, of one out of what seem several simultaneously possible objects of trains of thought. Focalization, concentration of consciousness, are of its essence. It implies withdrawal from some things in order to deal effectively with others.
Cellular studies of the posterior parietal cortex in monkeys have provided important insight into the neural mechanisms of focusing attention on specific objects in the visual field. Like neurons in other visual processing centers, each parietal neuron fires when a visual stimulus enters its receptive field (see Chapter 25 for a description of the receptive fields of cortical neurons in the visual system). The strength of the neuron's response depends on whether the animal is paying attention to the stimulus. The response is moderate when the animal's gaze is directed away from the stimulus but vigorous when the monkey attends to the stimulus (Figure 17–15).
Neurons in the posterior parietal cortex of a monkey respond more vigorously to a stimulus when the animal is attentive to the stimulus.
(Reproduced, with permission, from Wurtz, Goldberg, and Robinson 1982.)
A. A spot of light elicits only a few action potentials in a cell when the animal's gaze is directed away from the stimulus.
B. The same cell's firing increases when the animal's eyes move to the stimulus.
C. The cell's firing increases even more when the monkey touches the spot without moving his eyes.
These findings are consistent with the clinical observation that the parietal cortex is involved in focusing on objects in space. The response of the neuron is independent of how the animal attends to the stimulus. The firing rate of the neuron increases by about the same amount whether the animal merely looks at the stimulus or reaches for it while continuing to look elsewhere (Figure 17–15). This independence is significant because the posterior parietal cortex makes connections with structures in the prefrontal cortex that are involved in the planning and execution of movements of the eyes and hands.
When an object induces slightly disparate images in the two retinas, we do not see double images. Instead we perceive a single object in front of or behind the plane of fixation. Three-dimensional movies and Magic Eye books take advantage of this phenomenon, displaying slightly different images to each eye to induce a conscious perception of depth. Neurons in the primary visual cortex, the first synaptic relay of the visual system in the cerebral cortex, are sensitive to this retinal disparity and could therefore provide the basis for depth perception. However, these same neurons respond differently to black and white images that are anticorrelated and disparate—images in which each black pixel presented to one eye corresponds to a white pixel in the other, and vice versa. Although the neural synapse should give rise to a conscious perception of depth, in fact such images are not perceived as a single image having depth; instead they are treated as rivalrous alternating images. One sees either a white-on-black or black-on-white image, and the perceptual switch occurs spontaneously every few seconds, without any separation of depth.
Both retinal disparity and anticorrelated images produce an ocular reflex that adjusts the eyes to a depth of field equal to the plane of the image fixated, yet anticorrelated images are not perceived as one image with a single depth of field. The signal of depth triggers a cellular response in the primary visual cortex that is not consciously perceived and therefore does not have a direct role in conscious depth perception. It is thought that later stages of visual processing are responsible for depth perception and somehow reject the depth information computed for anticorrelated images in the primary visual cortex.
The study is important because it shows how neural activity can be dissociated from conscious perception. Disparate anticorrelated images are consciously perceived as rivalrous images—you see one input or the other but you do not see them fused into one object. However, neurons in the primary visual cortex do detect the anticorrelated images as fused and compute the depth of the fused image. In addition, the eyes make automatic vergence movements to the computed depth of the fused image that the brain does not consciously perceive.
These findings reinforce the idea that sensory input alone does not give rise to consciousness; higher-level interpretation of that input is needed.
How Is Self-Awareness Encoded in the Brain?
If visual attention is presently the most tractable example of consciousness, self-awareness is probably the deepest problem. Although aspects of self-awareness are evident in nonhuman primates, self-awareness is central to human identity and has evolved in parallel with language and other forms of symbolic communication.
A more promising approach to the study of consciousness may lie in the latest advances in neural prosthetics that give people the ability to voluntarily modulate neural signals to achieve a goal (move a cursor on the screen). Similarly, some individuals can achieve great control of their breathing and heart rate. These feats suggest that studies of how people can consciously control signals that are normally unconscious may shed light on the neural processes of self-awareness.