Hostname: page-component-745bb68f8f-b6zl4 Total loading time: 0 Render date: 2025-02-05T16:55:24.005Z Has data issue: false hasContentIssue false

The chemosensory brain requires a distributed cellular mechanism to harness information and resolve conflicts – is consciousness the forum?

Published online by Cambridge University Press:  24 November 2016

Richard Lathe*
Affiliation:
Division of Infection and Pathway Medicine, University of Edinburgh, Little France, Edinburgh EH16 4SB, United Kingdom. richardlathe@ed.ac.uk Pieta Research, Edinburgh EH10 5YW, United Kingdom State University of Pushchino, 142290 Pushchino, Russia.

Abstract

The central nervous system (CNS) evolved from a chemosensory epithelium, but a simple epithelium has limited means to resolve conflicts between early drives (e.g., approach vs. avoid). Understanding the role of “consciousness” as a resolution device, with specific focus on chemosensation and the olfactory system, is of appeal. I argue that consciousness is not the adjudicator, but is instead the forum that brings conflicting (conscious) inputs into a form that allows them to be (unconsciously) compared/contrasted, guiding rational action.

Type
Open Peer Commentary
Copyright
Copyright © Cambridge University Press 2016 

It was previously argued (Merrick et al. Reference Merrick, Godwin, Geisler and Morsella2014; Shepherd Reference Shepherd2007) that olfaction is central to understanding consciousness. In the target article, Morsella et al. extend this framework and argue that consciousness “is for adaptive ‘voluntary’ action” (sect. 2.4, para. 1), including “action selection” and the integration of conflicting inputs. In addition, they assert that “olfaction provides the best portal for understanding the neural correlates of additions to the conscious field” (sect. 3.5, para. 9). Their account is very welcome; I suggest possible additions to their narrative that might strengthen their case.

That chemosensation, notably olfaction, is central to understanding brain function recognizes that the vertebrate brain has its evolutionary origins in a simple chemosensory epithelium (Nieuwenhuys et al. Reference Nieuwenhuys, Ten Donkelaar and Nicholson1997). To this, one must add that a divergence occurred early in vertebrate evolution, with the olfactory/taste/vomeronasal systems becoming responsible for sensing external chemical stimuli (exteroception), whereas the limbic system (a derivative of the olfactory system) senses the internal milieu (Lathe Reference Lathe2001; Riss et al. Reference Riss, Halpern and Scalia1969). This view (limbic enteroception) is supported by evidence that acquired responses can be guided by internal body states, which are abolished by hippocampal lesions, and by molecular evidence that the hippocampus is selectively adorned with receptors for hormones and metabolites (Lathe Reference Lathe2001). Therefore, if olfaction plays a central role in consciousness, so too must the limbic system (e.g., Behrendt Reference Behrendt2013).

Regarding consciousness, we are undoubtedly “aware” of both external stimuli (tastes, smells) and internal stimuli (e.g., blood glucose and oxygen levels; see subsequent discussion). It should be noted that goal-oriented cravings of the hunger type are not restricted to calories (low blood glucose), and specific hungers can be driven by deficiencies in vitamins and specific minerals (Denton Reference Denton1982). Other hippocampal inputs monitor other body states relevant to immunity and reproduction. However, exactly as for odors, perception of the millions of molecules to which we are constantly exposed both internally (and externally) remains subliminal; we only become conscious of internal states (e.g., sickness, stress, hunger, etc.) when these (or their lack) surpass a threshold. In addition, we are surely aware of other factors, such as the time of day,Footnote 1 possibly also via the hippocampus (Lathe Reference Lathe2001).

Hence, to the central model of Morsella et al.: A hypothetical organism resides in a warm cave, and perceives an opening from which it could exit. The authors expand: “but then it perceives a noxious smell (e.g., smoke) from within the enclosure. Because of this new conscious content, it now exits hesitantly through the opening, even though it was inclined to remain within the warm enclosure” (sect. 1.3, para. 2). Later in their text, this scenario is revisited, and Morsella et al. observe that “the conscious content about the smell triggers a conscious content representing an avoidance tendency toward the smell” (sect. 5, para. 7).

The reader will perceive the following problem: Smoke is not necessarily aversive (smoked salmon is a delicacy, and many deem the odor of aromatic pipe tobacco to be attractive). The key word is “noxious.” Why does this creature avoid the smoke? How does the creature “know” that smoke is toxic? Two different scenarios present themselves.

  1. 1. The chemoreceptors for smoke components in this creature have been selected, over millions of years of evolution, to be wired up as innately aversive – in the same way that we respond reflexively with disgust and aversion to highly toxic H2S.;>Or,

  2. 2. The creature, remaining in the cave (i) perceives both the smoke (exteroception) and the adverse effects of exposure to molecules accompanying the smoke, notably CO and CO2, but also volatile organic compounds. (ii) The creature then becomes conscious of feeling sick and dizzy as a result of anoxia and toxemia (enteroception). Then, (iii) the creature makes an (unconscious) inference that the new smell is associated with the new sickness. Finally, (iv) it takes the decision to leave the cave.

If we were asked which of these processes best equates to the function of consciousness, we would probably say “decision-making based on comparing memory against sensation.” Or, in the terms of Morsella et al., action selection from multiple inclinations.

However, consciousness is distinct from both decision-making and memory. There is evidence that decisions are taken many seconds before they become available to consciousness (e.g., Soon et al. Reference Soon, Brass, Heinze and Haynes2008). Furthermore, consciousness is not memory either; we are only aware of a tiny subset of memory traces at a time. In other words, the consciousness circuits must be different from the sensory and memory circuits.

In addition, an important component of consciousness is “what one is thinking about.” This is clearly guided by internal and external sensory inputs. For example, if I am hungry, I think about food – where it might be found, how to procure it (even while I am engaged in another activity such as walking to work). But if I trip and fall, in subsequent actions pain takes precedence over hunger. Guided selection of what we are thinking about is central to consciousness.

I venture that consciousness might best be thought of as the forum in which relevant current and former experiences and associations are borne in mind and cogitated upon, but it does not itself take the decision.

I would liken the overall process of decision-making to a trial, where the relevant evidence is assembled and deliberated upon in a single “place” (the forum or court – consciousness), including access to the different accounts and previous relevant decisions from the legal archive (memory), such that the judge and jury, interacting in camera (unconscious), can hand down a ruling to the forum (conscious mind) – that dictates action at the same time as it becomes conscious. This would require several different circuitries operating in parallel.

In short, I feel that the joint focus on consciousness, chemosensation, and conflict resolution that Morsella et al. propose is an excellent step in the right direction. However, I add the caveat that the circuitries/mechanisms may be subdivided into several subsets that fulfill different functions – conscious assembly (Forum), memory (Archive), and unconscious decision-making (Judge and Jury) – and that consciousness alone does not resolve conflicts.

Footnotes

1. We are also conscious of time of day, and that this can dictate when an action is appropriate or inappropriate. One is reminded of Gallistel's bees, which, encountering a garden breakfast table one morning, return exactly 24 hours later in the expectation that marmalade will again be on the table (Gallistel Reference Gallistel1993).

References

Behrendt, R. P. (2013) Conscious experience and episodic memory: Hippocampus at the crossroads. Frontiers in Psychology 4, article 304. (Online journal). doi:10.3389/fpsyg.2013.00304.CrossRefGoogle ScholarPubMed
Denton, D. A. (1982) The hunger for salt: An anthropological, physiological and medical analysis. Springer.Google Scholar
Gallistel, C. R. (1993) The organization of learning. MIT Press.Google Scholar
Lathe, R. (2001) Hormones and the hippocampus. Journal of Endocrinology 169:205–31.Google Scholar
Merrick, M. C., Godwin, C. A., Geisler, M. W. & Morsella, E. (2014) The olfactory system as the gateway to the neural correlates of consciousness. Frontiers in Psychology 4, article1011. (Online journal). doi:10.3389/fpsyg.2013.01011.Google Scholar
Nieuwenhuys, R., Ten Donkelaar, H. J. & Nicholson, C. (1997) The central nervous system of vertebrates. Springer.Google Scholar
Riss, W., Halpern, M. & Scalia, F. (1969) Anatomical aspects of the evolution of the limbic and olfactory systems and their potential significance for behaviour. Annals of the New York Academy of Sciences 159:1096–111.Google Scholar
Shepherd, G. M. (2007) Perspectives on olfactory processing, conscious perception, and orbitofrontal cortex. Annals of the New York Academy of Sciences 1121:87101.Google Scholar
Soon, C. S., Brass, M., Heinze, H.-J. & Haynes, J. D. (2008) Unconscious determinants of free decisions in the human brain. Nature Neuroscience 11:543–45.Google Scholar