Introduction
Subjective experience is probably not limited to humans: The evidence from neurobiology and behavior

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Abstract

In humans, conscious perception and cognition depends upon the thalamocortical (T-C) complex, which supports perception, explicit cognition, memory, language, planning, and strategic control. When parts of the T-C system are damaged or stimulated, corresponding effects are found on conscious contents and state, as assessed by reliable reports. In contrast, large regions like cerebellum and basal ganglia can be damaged without affecting conscious cognition directly. Functional brain recordings also show robust activity differences in cortex between experimentally matched conscious and unconscious events. This basic anatomy and physiology is highly conserved in mammals and perhaps ancestral reptiles. While language is absent in other species, homologies in perception, memory, and motor cortex suggest that consciousness of one kind or another may be biologically fundamental and phylogenetically ancient. In humans we infer subjective experiences from behavioral and brain evidence. This evidence is quite similar in other mammals and perhaps some non-mammalian species. On the weight of the biological evidence, therefore, subjectivity may be conserved in species with human-like brains and behavior.

Introduction

Some years ago a popular book suggested that conscious cognition emerged 2500 years ago, between the writing of the Illiad and the Odyssey (Jaynes, 1976). Jaynes’ criterion of consciousness was whether Homer’s heroes talked to themselves—the warriors of the Illiad did not, while Odysseus did. But speech is not a necessary condition for consciousness. After all, aphasics with impaired inner and outer speech show no sign of losing consciousness. This Special Issue of Consciousness and Cognition explores extensive evidence that consciousness is a major biological adaptation going back many millions of years.

Subjective consciousness is of course inferred from observable evidence, much like working memory or other scientific constructs like electrons (Banks, 1995). Thus consciousness is not a metaphysical absolute, but a scientific construct like any other. In humans, the standard behavioral index of conscious cognition is accurate or verifiable report. It has been used scientifically since the beginning of psychophysics in the 1820s. Accurate report is highly reliable, but of course it is subject to limitations like any other empirical measure (Baars, 1988). However, behavioral measures of conscious cognitions are reliable enough to be routinely used in optometry, audiology, and the design of video screens and audio equipment. Physicians routinely use such evidence to test patients for impaired consciousness. Thousands of human experiments use verifiable report to study conscious perception, episodic memory, explicit cognition, focal attention, and the like (Baars, Banks, & Newman, 2004). But behavioral evidence is less useful when we study the question of animal consciousness. Bees meet the “accurate report” criterion when they convey information about food sources by doing a “waggle dance.” But human-like consciousness seems implausible in bees. Thus when we look beyond the human species, brain evidence may be a more useful source of evidence.

Can we infer subjectivity in other mammals? It is an inferential leap for one person to believe in the consciousness of another. Such inferences are made routinely when physicians test head-injured patients with impaired responsiveness. But if we make such inferences to other humans, then why not to other creatures, if the objective basis is the same? It is sometimes argued that animal subjectivity is not a testable claim, but we now have a number of studies that have tested such inferences, for example, on the question of visual consciousness in monkeys (e.g., Cowey & Stoerig, 1995). When we include other kinds of sensory awareness (especially touch, hearing, and pain) the circle of conscious animal species seems to grow larger. Non-mammals have been studied in less detail, but the range of conscious species will likely expand as we learn more.

Section snippets

Articles in this issue of Consciousness and Cognition

This issue is dedicated to the memory of Donald R. Griffin (see the obituary by Speck, 2005). Donald Griffin devoted his life to field studies of animals, and took intense criticisms from scientific colleagues when he began to address the question of animal consciousness—initially phrased as “animal cognition.” He was a scientific pioneer of outstanding courage and integrity, and we owe him a great debt of gratitude.

Jaak Panksepp is another modern pioneer, in his case in the study of the brain

The rediscovery of consciousness

Charles Darwin wrote that “Consciousness appears to be the product of complexity of organization,” an hypothesis that continues to draw serious scientific attention today (e.g., Edelman and Tononi, 2000, Tononi and Edelman, 1998). In the 19th century scientists like Darwin treated consciousness as an obvious scientific topic. Research on conscious sensory perception, conscious and unconscious influences on memory, selective attention, and even hypnosis began in 1800s. The 1400 pages of William

Behavioral and brain evidence

It is essential to distinguish between “intelligence” (as problem solving) and “consciousness” (as wakeful alertness and conscious perception, including the perception of pain and pleasure). We know of hundreds of differences between humans and other mammals in problem-solving tasks, ranging from word retrieval to migratory travel. Problem-solving tends to be species-specific. Early in life humans all over the world are able to learn a very large vocabulary, demonstrating a distinct

Behavioral indices of consciousness: Accurate report

In humans, the standard observational index of consciousness is “accurate or verifiable report” (e.g., Baars, 1988, Baars, 1998, Baars et al., 2004). In humans reports of conscious experiences do not have to be verbal; pressing a button, or any other voluntary response, is routinely accepted as adequate in research. Reporting responses are equally useful in animals.

Humans are extraordinarily good in detecting conscious sensory events. Seeing a single star on a dark night has been calculated to

The “commentary key” as evidence for mammalian consciousness

Skeptics sometimes question whether the ability of monkeys and cats to accurately report sensory events really involves conscious perception. That hypothesis can be tested in a number of ways. Recent research in macaques and other species is especially remarkable, because it allows us to ask if the animals studied respond to conscious events differently than they do to comparable brain events that are unconscious. Weiskrantz (1991) and Cowey and Stoerig (1995) have developed a “commentary key”

Other behavioral evidence

A number of other behavioral sources of evidence suggest consciousness. For example, mere distractibility in animals indicates a limited capacity for competing sensory streams, a well-established feature of conscious but not necessarily unconscious input processes (e.g., Baars, 1988, Baars, 1998, Baars et al., 2004). Simply presenting a distracting stimulus when an animals appears to be orienting to an event of interest creates competition between the two sources of information. Such

Electrical activity

It has been known since the late 1920s that there is a major difference in scalp electrical activity (EEG) between waking consciousness and deep, unconscious sleep, as reported by human subjects. These EEG phenomena apply to humans and other mammals alike, so much so that mammalian EEG studies are often applied to humans. In all mammalian species studied waking shows fast, irregular, and low-voltage field activity throughout the thalamocortical core. In contrast, deep sleep reveals slow,

Neuroanatomy of consciousness

In years past it was commonly said that consciousness must be some vague and non-specific aspect of the human brain. In fact, the waking state can be abolished by less than cubic centimeter lesions in the brainstem reticular formation and even smaller bilateral cuts in the intralaminar nuclei of the thalami (Bogen, 1995, Moruzzi and Magoun, 1949). In contrast, very large volumes of cortex can be lost without impairing the state of consciousness. Entire hemispheres are routinely removed

The thalamocortical (T-C) complex

In humans the thalamus and cortex are crucial for supporting the contents of consciousness (Edelman & Tononi, 2000). Thalamus is often considered to be an extension of cortex, an added sandwich of interacting layers that controls most traffic to and from cortex. Local damage to cortical sensory regions, like the fusiform gyrus for face perception, results in a loss of conscious knowledge about faces but not about other visual features like color, location, or size. If the intralaminar nuclei of

Visual consciousness in human and mammalian cortex

In the last 20 years we have made considerable progress on understanding perceptual consciousness in humans and other mammals. We have already discussed studies of blindsight in the macaque, suggesting that these primates have qualitative conscious visual experiences that closely resemble human visual experiences. Along the same lines, in a landmark series of multiple-neuron recording studies, Logothetis and colleagues have used binocular rivalry at different levels of visual analysis to track

Neurochemistry

In all mammals, waking, sleeping, and dreaming are controlled by brainstem nuclei that widely project their axons to the forebrain, secreting neuromodulators widely to the forebrain. Hobson (1997) writes that “in waking, the aminergic systems of the brain stem are spontaneously, continuously, and responsively active; in REM (rapid eye movement state), they are shut off by an active inhibitory process that is probably gaba-ergic. As a function of this shut-down of aminergic systems in REM, the

Functional evidence: In mammals, all goal-directed survival and reproductive behavior takes place during the conscious waking state

Mammalian locomotion, hunting, evasive action, exploring, sensing, actively attending, learning, eating, grazing, nursing, mating, social interaction, and all other goal-directed survival and reproductive actions take place only during waking, as defined by EEG and other indices. Perceptual consciousness, as defined objectively by recent brain research, only takes place during waking periods. It therefore appears that brain activity that supports consciousness is a precondition for all

Consciousness beyond mammals

What about non-mammals? The gross anatomy of bird brains they seems different from mammals. Like most non-mammals, birds have collections of nuclei rather than the beautiful fiber radiations of the thalamus into cortex. But gross-level nuclei could still have neuronal connectivities that are similar to the T-C system. At the level of neurons there is interesting evidence suggesting homologies. Some birds certainly pass the behavioral test. Irene Pepperberg’s African Grey Parrot Alex is able to

Summary

Cumulative evidence suggests that consciousness is a fundamental biological adaptation. The known brain correlates of consciousness appear to be ancient phylogenetically, going back at least to early mammals. In all mammals alertness and sensory consciousness are required for the goal-directed behaviors that make species survival and reproduction possible. In all mammals the anatomy, neurochemistry and electrical activity of the brain in alert states show striking similarities.

After more than

References (42)

  • B.J. Baars

    How does a serial, integrated and very limited stream of consciousness emerge from a nervous system that is mostly unconscious, distributed, parallel and of enormous capacity?

    Theoretical and Experimental Studies of Consciousness, Ciba Foundation Symposium

    (1993)
  • N. Block

    On a confusion about the function of consciousness

    Behavioral and Brain Sciences

    (1995)
  • A.L. Blumenthal

    Wilhelm Wundt—The founding father we never knew

    Contemporary Psychology

    (1979)
  • C. Cirelli et al.

    Neuronal gene expression in the waking state: A role for the locus ceruleus

    Science

    (1996)
  • A. Cowey et al.

    Blindsight in monkeys

    Nature

    (1995)
  • F.H.C. Crick et al.

    A framework for consciousness

    Nature Neuroscience

    (2003)
  • A. Destexhe et al.

    Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep states

    The Journal of Neuroscience

    (1999)
  • G.M. Edelman

    Naturalizing consciousness: A theoretical framework

    Proceedings of the National Academy of Sciences of the United States of America

    (2003)
  • D.B. Edelman et al.

    Identifying hallmarks of consciousness in non-mammalian species

    Consciousness and Cognition

    (2005)
  • G.M. Edelman et al.

    Degeneracy and complexity in biological systems

    Proceedings of the National Academy of Sciences of the United States of America

    (2001)
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    I am most grateful to Dr. Gerald M. Edelman and his colleagues at The Neurosciences Institute in San Diego for numerous discussions that have helped to strengthen this special issue of Consciousness and Cognition.

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