Minimal Neuroanatomy for a Conscious Brain: Homing in on the Networks Constituting Consciousness

Abstract

There is a consensus that consciousness is constituted by only a subset of all neuroanatomical regions and processes, but no agreement exists regarding which particular subset(s) constitutes it. We propose that a consensus will be reached if investigators (a) pool their knowledge regarding the regions whose non-participation does not in principle render the nervous system devoid of consciousness (e.g., the cerebellum, amygdalae, hippocampi, hemispheric commissures, ‘pre-cortical’ thalamus, and vast regions of the cortex), and (b) focus on the long-overlooked olfactory system. This ‘brutally-reductionistic’ approach may isolate the physical basis of consciousness; even its falsification would help to illuminate this enigma.

Remarkable empirical advances have led to the consensus that consciousness¹ is associated with only a subset of all neuroanatomical regions and processes, but no agreement exists regarding which particular subset(s) embodies the physical events (presumably networks) capable of constituting consciousness. At one extreme, researchers propose that consciousness can be constituted at a small scale, by a unique set of cells in particular regions (Koch 2004); at the other extreme, researchers propose that it requires large-scale synchronization of ‘equipotential’ elements across the brain (Greenfield 2000). A consensus will be reached if investigators (a) pool their knowledge regarding the capacious catalog of regions whose non-participation does not render the nervous system incapable of still exhibiting an identifiable form of consciousness, and (b) focus on the long-overlooked physical basis of olfactory consciousness.

There are numerous neuroanatomical regions that do not render the nervous system incapable of continuing to exhibit an identifiable form of consciousness when they are non-participatory (e.g., extirpated or inactivated). Cataloging such regions prevents researchers from barking up the wrong tree when attempting to isolate the physical basis of consciousness. Through the process of elimination, such a catalog also helps one distill what can be conceptualized as the minimal neuroanatomy for a conscious brain. The following are conservative, a-theoretical conclusions from such a catalog.

Gross Anatomy

Although the absence of the spinal cord or cerebellum leads to sensory, motor, and even cognitive deficits, it does not seem to eradicate all forms of consciousness. Similarly, although extirpation of the amygdalae or hippocampi leads to anomalies including deficits in affective processing and episodic memory, respectively, it seems that an identifiable form of consciousness persists without these structures. This is not to imply that these structures are incapable of generating a form of consciousness, but only that, in principle, a brain can be a conscious brain without them. With respect to these structures and those listed below, our approach is valid only if consciousness does not require some hitherto unidentified, large-scale interaction requiring a subset of the regions that are thus ‘conceptually extirpated.’ If the approach is proved to be invalid, then there will be strong evidence that consciousness does require multiple regions (Greenfield 2000), and much will have been learned regarding its physical nature.

Investigations on ‘split-brain’ patients and split-brain patients experiencing binocular rivalry (O’Shea and Corballis 2005) suggest that a conscious brain does not require the non-dominant (usually right) cerebral cortex nor the cerebral commissures. Investigations regarding prefrontal lobe syndromes (Gray 2004) and the psychophysiology of dreaming, which involves prefrontal deactivations (Muzur, Pace-Schott, and Hobson 2002), suggest that, although the prefrontal lobes are involved in cognitive control, they are not essential for the generation of consciousness, consistent with the view that cognitive control and consciousness are distinct processes (Koch and Tsuchiya 2007).

Investigators have challenged the prevalent view that the cortex should be construed as the organ of consciousness. As noted in Merker (2007), Wilder Penfield concluded from observations of awake patients undergoing brain surgeries involving ablations and direct brain stimulation that, although the cortex may elaborate the contents of consciousness, it is not the seat of consciousness. Based on such evidence and clinical observations of anencephaly, Merker (2007) re-introduces this hypothesis in a framework in which consciousness is primarily a phenomenon associated with mesencephalic areas. It seems that consciousness can persist even when great quantities of the cortex are absent. The question now is whether an identifiable form of consciousness can exist despite the non-participation of all cortical matter.

The Case for Olfaction

To understand the neural basis of consciousness, researchers have followed Sir Francis Crick’s recommendation and focused on the visual system, but this dominant, neuroanatomically vast, and far from primitive modality may not be the easiest arena for our reductionistic approach. Olfaction is better suited for such purposes. For example, it is tempting to hypothesize that a conscious brain requires thalamocortical interaction between thalamic ‘relay’ neurons and cortex, but this is inconsistent with the fact that we consciously experience aspects of olfaction even though olfactory afferents bypass the thalamus and directly target regions of the ipsilateral cortex. This is not to imply that the relay thalamus is unnecessary for other forms of consciousness (e.g., visual or auditory) or that a conscious brain experiencing only olfaction does not require the thalamus: in post-cortical stages of processing, the thalamus receives inputs from cortical regions involved in olfaction.

The neural correlates of conscious olfactory perceptions, imagery, and hallucinations, as revealed by direct stimulation of the brain, neuroimaging, and lesions, suggest that olfactory consciousness does not require the olfactory bulb (Mizobuchi et al. 1999). It seems that patients can still experience explicit, olfactory memories following bilateral olfactory bulbectomies, though definitive evidence is wanting. It seems that the minimal neuroanatomy for consciousness does not require the relay thalamus nor at least one structure (the olfactory bulb) proposed to serve a function similar to that of the relay thalamus (Kay and Sherman 2007).

In addition to its relatively simple, neuranatomically accessible, and phylogenetically-primitive structure, olfaction is well-suited for consciousness research because of its phenomenological characteristics: unlike most other modalities, it regularly yields no subjective experience of any kind when the system is understimulated, as during sensory habituation or when odorants are subliminal (as in blind-smell; Bensafi et al. 2004). This ‘experiential nothingness’ (an informative baseline condition for consciousness research) is more akin to the phenomenology of the blind spot than to that which is experienced when visual stimulation is absent (darkness).

A critical question is whether the olfactory system can generate some form of consciousness (a ‘microconsciousness,’ as in Semir Zeki’s work; Koch, 2004) by itself or whether olfactory consciousness requires interactions with non-olfactory regions of the minimal brain proposed above. Perhaps one becomes conscious of olfactory percepts only when they ‘cross-talk’ with other systems or when they influence processes that are motor (Bensafi et al., 2004) or semantic-linguistic (Herz 2003). According to Buck (2000), conscious aspects of odor discrimination depend primarily on the activities of the frontal and orbitofrontal cortices; according to Barr and Kierman (1993), olfactory consciousness depends on the pyriform cortex. These proposals appear inconsistent with subcortical accounts of consciousness (Merker 2007). Research on phantosmias and explicit versus implicit olfactory processing may resolve this discrepancy. Hence, it is critical to identify the minimal region(s) whose stimulation is sufficient to induce olfactory hallucinations.

Therefore, the minimal neuroanatomy for a conscious brain need not in principle include the spinal cord, cerebellum, amygdalae, hippocampi, pre-cortical relay thalamus, hemispheric commissures, non-dominant cortical hemisphere, nor many portions of the dominant hemisphere. Hypothetically, consciousness can be instantiated in a minimal nervous system without these regions and their associated processes. This hypothesis can be falsified if the remaining areas alone are insufficient to constitute consciousness, perhaps because the physical basis of consciousness lies outside these regions, or consciousness requires a larger scale network (Greenfield 2000). Such a falsification would advance research on consciousness. Through multidisciplinary research, the subset(s) of regions constituting consciousness may be further isolated by eliminating regions of this minimal brain.