Colorado Neurological Institute
Denver, CO, USA
Full paper available at http://www.phil.vt.edu/assc/newman/
Crick's "Searchlight Hypothosis"
Crick and Koch's Theory of "40-Hz" Binding
Llinas' et al's Theory of 40-Hz Scanning.
Taylor's Model of Reticular Nucleus Global Guidance
Baars' (1988) Extended Reticular-Thalamic Activation System
Recent extensions of the ERTAS model
Parallel to the general renaissance of the study of consciousness over the past decade has been a renewed interest in the contributions of subcortical structures of the CNS to functions such as selective attention, memory, neural binding, etc. Situated at the center of the brain, the thalamus has become increasingly implicated in functions related to the global integration of cognitive processes. This paper provides a brief historical review of the anatomy and functions of the thalamus, and its integral relations with cortical systems mediating cognition. I then introduce recent models of the thalamocortical system bearing on the topic of the seminar.
FIGURE 1. The thalamus of one hemisphere of the brain. The thin layer of neurons partially surrounding the thalamus is the reticular nucleus. (from LaBerge, 1995, p. 161)
It has been known since the 19th century that the sensory tracts for vision, hearing and touch synapse upon specific nuclei in the thalamus. These nuclei, in turn, send topographic projections to the primary sensory areas of the neocortex.
William James (1890) expressed the consensus of the science of his time when he asserted that "the cortex is the sole organ of consciousness in man" (p. 66). In this scenario, the "lower centers" are repositories of instinctual and biological functions, although the thalamus has the privileged position of being the "relay station" for information streaming into the cortex from the outside world.
James (1890) wrote eloquently about the "stream of consciousness", and the centrality of attention in conscious mentation. Given his prescience in so many areas, one might have expected him to speculate on the possible significance of the thalamus in filtering this "stream" via the "synaptic cleft" it provides. But with his characteristic frankness, he admitted to the science of his time having a "shadowy view ... If it has no other advantage, it at any rate makes us realize how enormous are the gaps in our knowledge, ....(p. 80)
These gaps did not deter James from discussing consciousness as a natural phenomenon,however. Both as a psychologist and philosopher, he shared the convictions of his contemporaries that "nothing was more essential to the mind than consciousness" and that, "The mind in all its activities and processes was ... transparent to itself; nothing was hidden from its inner view. (Dennett, 1987, p. 162). It was James (1980), of course, who coined the term "stream of consciousness", describing it as "a teaming multiplicity of objects and relations" - never simple sensation by itself - "and what we call simple sensations are the results of discriminative attention, pushed often to a very high degree." (p. 224). Characteristically, he further argued that consciousness was highly purposeful, a "fighter for ends", not simply a "detached observer". Millions of items of the outward order are present to my senses which never properly enter into my experience. Why? Because they have no interest for me. My experience is what I agree to attend to. Only those items which I notice shape my mind--without selective interest, experience is utter chaos. (p. 402)
For all his energy and eloquence, James' philosophy of science was singularly unsuccessful in swaying his "more modern" colleagues. By the time he died in 1910, two opposing names had come to dominate the intellectual landscape: Freud, who ventured where the previous generation expected nothing mental to exist, and found "the unconscious"; and J. B. Watson who declared the entire "Science of Mental Life" championed by James illusory.
The triumph of Behaviorism in this country had an interesting effect upon neuroscience between the two World Wars. The focus shifted from humans to animals, from "higher cortical" to subcortical "centers" (refer to Figure 2). Researchers discovered the centrality of the hypothalamus ("HY", Fig. 2) in regulating instinctual drives (privately referred to as the "4 Fs": fighting, feeding, fleeing and f---ing). Papez (1937) theorized that a labyrinth circle of tracts connecting the hypothalamus with the amygdala ("AM"), hippocampus and underside of the cerebral cortex, constituted an "emotional brain". Because the upper half of this Circle of Papez forms the "rim" (or limbus) of the inner surface of the hemispheres, this complex came to be known as the limbic system.
FIGURE 2. The thalamus sitting atop the brainstem at the center of the brain, surrounded by the basal ganglia and limbic structures. Most of the neocortex and white matter of the left hemisphere have been removed to reveal these subcortical structures. The thalamus lies closest to the midline of the hemisphere. The basal ganglia are situated more laterally (towards the outside). The amygdala (Am) and hippocampus lie on the medial (inner) surface of the temporal lobe. (from Newman, 1995a, p. 174)
The thalamus fills the center of this "donut" of limbic structures. Surprisingly, however, only a small minority of thalamic nuclei are truly "limbic." The great bulk of thalamic connections are with the neocortex (Note: keep in mind that only the gross anatomy of nuclei and cortical areas are portrayed in these figures, NOT the actual masses of connecting tracts/white matter, filling the space between the cortex and subcortical structures).
The thalamus is not simply the "relay station" for sensory information flowing toward the cortex; it is the cortex's chief source of extrinsic activation. Not only the primary areas for vision ("V1") audition ("A1"), and somatosensory ("S1") sensation (refer to Figure 3), but association cortex as well, share orderly projections with particular thalamic nuclei. The thalamus also has "motor" ("M1", "MA") projections to the frontal lobes. I place "motor" in quotes because these nuclei are actually relays for inputs from deep in the basal ganglia (refer to Figure 2). The functions of these structures are so integral to the thalamocortical system, that Imust briefly summarize them.
FIGURE 3. The major divisions of the thalamus and the major projections it shares with the cerebral cortex. Thalamic nuclei (left- side): A-anterior nucleus; MD-medialdorsal nucleus; MI-massa intermedia; nRt-nucleus reticularis thalami. Thalamocortical projection areas: A1-primary auditory cortex; CG-cingulate gyrus; IPL-inferior parietal lobule; M1- primary motor cortex; MA-motor association cortex; MB- mamillary body; PfC-prefrontal cortex; S1-primary somatosensory cortex; SPL-superior parietal lobule; V1-primary visual cortex; VA-visual assocation cortex. (from Newman, 1995a. p. 178)
The basal ganglia (BG) and hippocampus are recipients of inputs from wide areas of cortex. As Figure 2 suggests, BG inputs originate most richly from frontal cortex; while projections to the hippocampus come largely from posterior cortex. Edelman (1989) characterizes these two subcortical structures as "cortical appendages and organs of succession". For the hippocampal system, the succession is of sense perceptions and the episodic memories these leave behind; for the BG system these entail the orderly succession of plans and choices, and the procedural memories associated with learned skills. The actions of this system really have no "point of origination", because the "cortico-basal ganglia- thalamo-cortical loop" (Parent and Hazrati, 1995) which mediates them (like the Circle of Papez) is a massive reverberatory circuit, modulating all motor outputs. Newman (in preparation) reviews evidence that portions of this circuit may provide the essential substrate for conscious volition.
Consistent with this hypothesis are the intricate "top-down" controls which pre-frontal cortex (PfC) is capable of exercising over BG, limbic and thalamic nuclei. Llinas and Pare (1991) have noted that the number of cortical projections back to thalamic nuclei are an order of magnitude greater those the cortex receives. In addition to the swath of projections PfC exchanges with the medial dorsal nucleus ("MD", Fig. 3), other pre-frontal projections directly influence limbic and brain stem circuits. Finally, PfC and BG send strategic sets of projections to a thin sheet of cells covering the outer surfaces of the two thalami, called the nucleus reticularis ("nRt", Fig. 3, also see "reticular nucleus", Fig. 1). This reticular complex is central to most of the models presented here.
Conclusion.These accumulated findings, and the models they have engendered, constitute an impressive framework for constructing a general theory of consciousness (An extended argument for this is made in Newman (in prep.), which was recently submitted to PSYCHE.)