(I would like to acknowledge a special debt of gratitude here to Dr. Jaak Panksepp, Dr. James Rose and Dr. David Edelman, for their patience in answering my queries. Any errors here are entirely my own.)
Neural pre-requisites for consciousness
Neuroscientists are accustomed to distinguishing two varieties of consciousness: a primary consciousness which involves having mental images of present events, and a higher-order consciousness which involves awareness of one's previous experiences, imagining new experiences and self-awareness. Primary consciousness is commonly ascribed to some (but not necessarily all) mammals, while higher-order consciousness is generally restricted to a much smaller group - typically humans and chimpanzees (Rose, 2002).
I shall confine my discussion here to primary consciousness. My interest lies in identifying the neural basis of consciousness, rather than in pursuing the philosophically problematic quest for the neural correlates of consciousness (NCC). My aim is to answer the following two questions:
Major properties of primary consciousness
According to Edelman, there are three major properties of consciousness that are fairly well accepted by neurobiologists (personal email, 19 July 2004):
During deep sleep, in persistent vegetative states, under anesthesia, and during epileptic absence seizures, EEG recordings show slow, high-amplitude, regular activity of the order of less than 4 Hz. This seems to be the case in the brains of all mammals from which such recordings have been made (Edelman, personal communication, 19 July 2004).
Kinds of conditions for consciousness: enabling, modulating and specific
Before we can evaluate the significance of these characteristics of consciousness, we need to distinguish the variety of senses of the term "condition for consciousness", which are discussed by Koch and Crick (2001):
It is important to distinguish the general, enabling factors in the brain that are needed for any form of consciousness to occur from modulating ones that can up- or down-regulate the level of arousal, attention and awareness and from the specific factors responsible for a particular content of consciousness (Koch and Crick, 2001).
(i) Enabling conditions for consciousness
The authors explicitly warn against assuming that enabling factors correspond to conscious states as such. One might as well argue that consciousness resides in the heart, since it rapidly ceases if the heart stops beating.
Consciousness hinges on neural activities occurring within the thalamocortical system (Tononi, 2004). This corresponds to the second of the three major properties enumerated by Edelman. Within the thalamus, the intralaminar nuclei can be described as enabling factors: acute bilateral loss of function in these small structures leads to immediate coma or profound disruption in arousal and consciousness (Koch and Crick, 2001).
(ii) Modulating conditions for consciousness
Among the brain's neuronal modulating factors is the reticular activating system (RAS), whose activities, which occur in nuclei within the brain stem and the midbrain, control the level of neurotransmitters in the thalamus and forebrain. Appropriate levels are needed for sleep, arousal, attention, memory and other functions critical to consciousness (Koch and Crick, 2001). As we saw above, the brain's EEG rhythms are the first of the three major properties enumerated by Edelman. Waking EEG patterns are characterised by fast, irregular, low-voltage field activity throughout the thalamocortical core, as well as complex interactions between neurons; while unconscious sleep shows slow, regular, synchronised EEG patterns and high-voltage field activity (Baars, 2001). Although these rhythms may appear to be nothing more than diagnostic features by which we can identify consciousness, they are actually manifestations of an underlying system in the brain (the RAS) which controls consciousness.
(iii) Specific conditions for consciousness
Neuroscientists still have little understanding of why activity in specific areas of the cortex generates different sensory modalities - e.g. why the auditory and visual cortex are associated with sound and colour respectively. The necessary and sufficient conditions for a specific content of consciousness remain elusive (Tononi, 2004), but are thought to be caused by specific neural activity in cortex, thalamus, basal ganglia and associated neuronal structures.
The role of the cerebral cortex
In human beings, a thalamus and reticular activating system are necessary but not sufficient conditions for primary consciousness, as shown by the fact that we are unaware of neural activity that is confined to the brainstem:
[A] large part of the activity occurring in our brain is unavailable to our conscious awareness (Dolan, 2000; Edelman and Tononi, 2000; Koch and Crick, 2000; Libet, 1999; Merikel and Daneman, 2000). This is true of some types of cortical activity and is true for all brainstem and spinal cord activity (Rose, 2002, p. 15).
Only when neural activity reaches the cerebral cortex - the extensive outer layer of grey matter in the brain's cerebral hemispheres - does it translate into conscious awareness. This region of the brain is believed to be largely responsible for sensation, voluntary muscle movement, thought, reasoning, and memory.
Destruction of the cerebral cortex leaves a human being in a persistent vegetative state, capable of behavioural wakefulness (e.g. eyes are open) but devoid of all conscious awareness. PVS patients are still capable of stereotypical responses to noxious stimuli (Rose, 2002, p. 13). Non-primate mammals whose cerebral hemispheres have been destroyed are capable of locomotion, postural orientation, elements of mating behavior, and fully developed behavioral reactions to noxious stimuli, but cannot survive without assisted feeding (Rose, 2002, p. 13).
The cerebral cortex is mostly made up of a six-cell-layered neocortex, technically known as isocortex. It is this laminated structure that supports consciousness in human beings:
Extensive evidence demonstrates that our capacity for conscious awareness of our experiences and of our own existence depends on the functions of this expansive, specialized neocortex. This evidence has come from diverse sources such as clinical neuropsychology (Kolb and Whishaw, 1995), neurology (Young et al., 1998; Laureys et al., 1999, 2000a-c), neurosurgery (Kihlstrom et al., 1999), functional brain imaging (Dolan, 2000; Laureys et al., 1999, 2000a-c), electrophysiology (Libet, 1999) and cognitive neuroscience (Guzeldere et al., 2000; Merikle and Daneman, 2000; Preuss, 2000).We are unaware of the perpetual neural activity that is confined to subcortical regions of the central nervous system, including cerebral regions beneath the neocortex as well as the brainstem and spinal cord (Dolan, 2000; Guzeldere et al., 2000; Jouvet, 1969; Kihlstrom et al., 1999; Treede et al., 1999) (Rose, 2002, p. 6).
The reasons why the neocortex is critical for consciousness have not yet been fully resolved. Human consciousness appears to require brain activity that is diverse, temporally conditioned and of high informational complexity. (This integrative requirement corresponds to Edelman's third major property of consciousness.) The neocortex satisfies these criteria because it has two unique structural features: (1) exceptionally high connectivity within the neocortex and between the cortex and thalamus; (2) enough mass and local functional specialisation to permit regionally specialised, differentiated activity patterns (Rose, 2002, p. 7).
The neocortex is divided into primary and secondary regions (which process low-level sensory information and handle motor functions), and the associative regions. Brain monitoring techniques indicate that in human beings, only processes that take place within the associative regions of the cortex are accompanied by consciousness; activities which are confined to the primary sensory cortex or processed outside the cortex are inaccessible to consciousness (Roth, 2003, pp. 36, 38; Rose, 2002, p. 15). Consciousness thus depends on the functions of the association cortex, not primary cortex. The associative regions are distinguished by their high level of integration and large number of connections with other regions of the brain (Roth, 2003, p. 38) - corresponding to Edelman's third major property of consciousness.
It is now believed that slow-wave sleep, coma and PVS cause a loss of primary (and phenomenal) consciousness precisely because in these states, the ability to integrate information between different regions of the cerebral cortex is greatly reduced (Tononi, 2004; Baars, 2003).
Which animals meet the neural conditions for consciousness?
The major subdivisions of the brain - spinal cord, hindbrain, midbrain, diencephalon, telelcephalon - are found in all vertebrates. The thalamus is also present. All vertebrate brains have a forebrain pallium, known as the cerebral cortex in mammals (Prescott, 1999, p. 9). To a limited degree, all vertebrates instantiate the first major property of consciousness described by Edelman (2004) above. To date, the reentrant interactions between thalamus, cortex and basal ganglia which characterise consciousness have only been found in mammals, but they may also occur in other vertebrates such as birds. More research needs to be done (Edelman, personal email, 19 July 2004).
While behavioural sleep is found in most animals, the EEG patterns in the brain which distinguish sleep from wakefulness are confined to mammals and birds. According to Baars (2001), "all mammalian species studied so far show the same massive contrast in the electrical activity between waking and deep sleep". Birds' waking EEG patterns resemble those of mammals; and their sleep patterns are very similar to those of mammals, except that REM sleep is shorter (Kavanau, 1997, p. 257; Cartmill, 2000; Edelman, personal email, 19 July 2004).
Although some mammals have much more neocortex in proportion to their body size than others, which probably explains the wide variation in different species' performance in problem-solving tasks, "the size of the neocortex seems[s] to be irrelevant to the existence of wakefulness and perceptual consciousness" among mammals (Baars, 2001).
What about other animals? It is here that comparisons break down. Among animals, only mammals possess a true neocortex (Rose, 2002, p. 10). Some authors have claimed that reptiles and birds have a primordial neocortex, but it does not have the layered structure found in the brains of mammals. Thus it is generally agreed that a fully developed neocortex is present only in mammals (Nieuwenhuys, 1998). Specifically, reptiles and birds do not appear to possess any brain structures possessing the special features of the association cortex - a high level of integration and a large number of connections with other regions of the brain.
The cerebellum is the only structure in the brains of non-mammals lack structures with a comparable ability to rapidly integrate diverse kinds of information. Interestingly, the cerebellum, located at the back of the brain, "contains probably more neurons and just as many connections as the cerebral cortex, receives mapped inputs from the environment, and controls several outputs", and yet "lesions or ablations indicate that the direct contribution of the cerebellum to conscious experience is minimal" (Tononi, 2004), and "removal of the cerebelleum does not severely compromise consciousness" (Panksepp, 1998, p. 311). The reason why activity in the cerebellum is not associated with consciousness is thought to be because different regions of the cerebellum tend to operate independently of one another, with little integration of information between regions (Tononi, 2004).
In the light of the above evidence, many authors are disposed to deny non-mammals any kind of conscious awareness (Edelman and Tononi, 2000; Rose, 2002, cites supporting authorities).
The massive dissimilarities between the neocortex (the presumed locus of conscious states) of the mammalian brain and the much more primitive structures in the brains of birds and reptiles, effectively undermine any arguments for conscious feelings in birds and reptiles that are based on "similarity" alone. We are forced to conclude:
Conclusion 4.33 The neural requirements for consciousness appear to include: (i) a unique reentrant pattern of interaction between the cerebral cortex, thalamus and basal ganglia; (ii) a reticular activating system (RAS) that supports wakefulness and sleep, which are distinguished by their fast-wave and slow-wave EEG patterns respectively; (iii) a high level of integration and a large number of connections between diverse regions of the cerebral cortex, such as is found in the associative regions of the cortex.
Conclusion 4.34 All mammals satisfy the neural requirements for consciousness to at least some degree. The brains of other animals are too different for us to say that they meet these requirements, as they lack a true neocortex.
Conclusion 4.35 Similarity arguments, taken by themselves, are not strong enough to warrant the ascription of conscious feelings to non-mammals.