Elsevier

Cognition

Volume 79, Issues 1–2, April 2001, Pages 135-160
Cognition

Consciousness and the brainstem

https://doi.org/10.1016/S0010-0277(00)00127-XGet rights and content

Abstract

In the first part of this article we summarize a theoretical framework and a set of hypotheses aimed at accounting for consciousness in neurobiological terms. The basic form of consciousness, core consciousness is placed in the context of life regulation; it is seen as yet another level of biological processing aimed at ensuring the homeostatic balance of a living organism; and the representation of the current organism state within somato-sensing structures is seen as critical to its development. Core consciousness is conceived as the imaged relationship of the interaction between an object and the changed organism state it causes. In the second part of the article we discuss the functional neuroanatomy of nuclei in the brainstem reticular formation because they constitute the basic set of somato-sensing structures necessary for core consciousness and its core self to emerge. The close relationship between the mechanisms underlying cortical activation and the bioregulatory mechanisms outlined here is entirely compatible with the classical idea that the reticular formation modulates the electrophysiological activity of the cerebral cortex. However, in the perspective presented here, that modulation is placed in the setting of the organism's homeostatic regulation.

Introduction

The terms consciousness and brainstem have long been associated on the basis of two lines of evidence. The first is the fact that damage to the upper brainstem is a known cause of coma and persistent vegetative state, the disease states in which consciousness is most severely impaired. The second line of evidence originates from classical experiments which suggested, either through lesions or electrical stimulation, that a part of the brainstem, known as the reticular formation, is associated with the electrophysiological pattern commonly found in wakeful and attentive states. Such evidence supported a general account of the relationship between brainstem and consciousness that can be summarized as follows: (a) the brainstem contains the reticular formation which is the origin of the ascending reticular activating system; (b) the engagement of the ascending reticular activating system activates the cerebral cortex; (c) the process of activating the cortex underlies wakefulness and attention; and (d) wakefulness and attention are indispensable constituents of consciousness, or, as some might say, constitute consciousness.

While there is little doubt that cortical activation due to brainstem engagement is an indispensable part of the conscious state, we believe that the above account is incomplete for a number of reasons. For example, the account dates from a time in which the phenomena of consciousness were conceptualized in exclusively behavioral, third-person terms. Little consideration was given to the cognitive, first-person description of the experience of the subject who is conscious. Moreover, the neuroanatomical view of the brainstem that informs this traditional account does not include recent advances in the description of different nuclei within the reticular formation and of their distinct connections to other brain regions, nor does it include the consequent revision of the concept of reticular formation. No less importantly, the account does not address the functional context in which the brainstem plays its presumed activation role. For example, what drives the brainstem to activate the cerebral cortex in the manner in which it does? Why is the activation system based on brainstem structures as opposed to other structures?

Recently, we have proposed that the role of the brainstem in consciousness can be seen in a new perspective, that of life regulation, and that the new perspective may help explain why and how brainstem nuclei exert their varied influences on structures located rostrally, namely on the cerebral cortex (Damasio, 1998, Damasio, 1999).

Some nuclei of the brainstem have long been linked to the regulation of life, along with nuclei in the nearby hypothalamus, but a link between nuclei that regulate life and the process of consciousness has not been proposed before. Likewise, the brainstem nuclei that have long been linked to consciousness, namely those of the reticular formation, have not been linked to the regulation of life. In terms of theoretical background, the critical feature of the proposal is the 3-way connection it proposes for consciousness, for the nuclei involved in homeostasis, and for the nuclei in the reticular formation.

The proposal specifies two closely related but separable problems in the investigation of consciousness. The first is the problem of understanding how the brain engenders the mental patterns we experience as the images of an object. By “object” we mean entities as diverse as a person, a place, a melody, or an emotional state; by “image” we mean a mental pattern in any of the sensory modalities, e.g. a sound image, a tactile image, the image of an aspect of an emotional state as conveyed by visceral senses. Such images convey the physical characteristics of the object as well as the reaction of like or dislike one may have for an object and the plans one may formulate for it, or convey the web of relationships of the object among other objects. This first problem of consciousness is the problem of how we form a temporally and spatially unified “movie-in-the-brain”, a metaphorical movie, of course, with as many sensory tracks as the brain's sensory systems. Solving this first problem in neuroscientific terms consists of discovering how the brain makes neural patterns in its neural circuits and turns those neural patterns into the explicit mental patterns of the whole range of possible sensory images, which stand for any object, any relationship, concrete or abstract, any word or any sign.

The second problem of consciousness concerns how, in parallel with creating mental patterns for an object, the brain also creates a sense of self in the act of knowing. The solution for this second problem requires the understanding of how each of us has a sense of “me”; of how we sense that the images in our minds are shaped in our particular perspective and belong to our individual organism. Solving the second problem of consciousness consists of discovering the biological underpinnings for the construction of the mental patterns which automatically convey the sense of a self. Importantly, the solution traditionally proposed for the problem, that of an homunculus creature who is in charge of knowing, is not acceptable. There is no homunculus.

The problem of how the movie in the brain is generated and the problem of how the brain also generates the sense that there is an owner and observer for that movie are so interrelated that the latter problem is nested within the former. The second problem is that of generating the appearance of an owner and observer for the movie, that materializes within the movie.

The new proposal specifies that we first become conscious when, in addition to being awake and capable of making sensory images of an object, our organisms internally construct and internally exhibit a specific kind of wordless knowledge – the knowledge that the organism has been changed by an object – and when such knowledge occurs along with the salient enhancement of the object image caused by attention being allocated to it.

The central question arising from this formulation is how this new knowledge begins to be gathered. The following hypothesis captures the solutions we propose to answer it: core consciousness (the simplest form of consciousness) occurs when the brain's representation devices generate an imaged, nonverbal account of how the organism's own state is affected by the organism's interaction with an object, and when this process leads to the enhancement of the image of the causative object, thus placing the object saliently in a spatial and temporal context. The protagonist of core consciousness is the core self, the simplest form of self.

The hypothesis outlines two component mechanisms: the generation of an imaged nonverbal account of an object-organism relationship, and the enhancement of the images of an object. The hypothesis is grounded on the following premises:

  • 1.

    That the organism, as a unit, is mapped in the organism's brain, within structures that regulate the organism's life and signal its internal states continuously; that the object is also mapped within the brain, in the sensory and motor structures activated by the interaction of the organism with the object; that both organism and object are mapped as neural patterns, in first-order maps; and that all of these neural patterns can become mental images.

  • 2.

    That the neural activity inherent in sensorimotor maps pertaining to the object cause changes in the neural activity of the maps pertaining to the organism.

  • 3.

    That the activities described in (2) can in turn be conveyed to second-order maps which thus represent the overall relationship of object and organism.

  • 4.

    That the neural patterns transiently formed in second-order maps can become mental images, just as is the case with the neural patterns in first-order maps, thus producing an image of the relationship between organism and object.

The organism referred to in the hypothesis is represented in the brain by a coherent collection of neural patterns which map, moment by moment, the state of the organism in its many dimensions. This ceaselessly maintained first-order collection of neural patterns is described in the proposal as the “proto-self”. The proto-self occurs not in one brain region but in many, at a multiplicity of levels, from the brainstem and hypothalamus to the cerebral cortex, in structures that are interconnected by neural pathways. These structures are intimately involved in the processes of regulating and representing the state of the organism, two closely tied operations. In short, the proto-self is a coherent collection of neural patterns which map, moment by moment, the state of the physical structure of the organism in its many dimensions.

It should be noted at the outset that the proto-self is not the sense of self in the traditional sense, the sort of self on which our current knowing is centered, that is, the core self (the protagonist of core consciousness), and the autobiographical self (the extended form of self which includes one's identity and is anchored both in our past and anticipated future). The proto-self is the pre-conscious biological precedent of both core and autobiographical self.

The proto-self should also not be confused with the homunculus of classical neurology. The proto-self does not occur in one place only, and it emerges dynamically and continuously from interacting signals originating at multiple levels of the nervous system. The proto-self is not an interpreter; it is a reference.

The structures required to implement the proto-self are as follows:

  • 1.

    Several brainstem nuclei which regulate body states and map body signals.

  • 2.

    The hypothalamus and the basal forebrain.

  • 3.

    The insular cortex, cortices known as S2, and the medial parietal cortices located behind the splenium of the corpus callosum, all of which are part of the somatosensory cortices.

The structures which are not required to implement the proto-self are as follows:

  • 1.

    Several early sensory cortices, namely those of areas 17, 18, 19, which are dedicated to vision; 41/42, 22, dedicated to hearing; area 37, which is partly dedicated to vision but is also a higher-order cortex, and the part of S1 concerned with fine touch. These cortices are involved in the making of modality-specific sensory patterns that support the mental images of diverse sensory modalities available in our mind. They play a role in consciousness inasmuch as the images of the object-to-be-known are assembled from these regions, but they play no role in the proto-self.

  • 2.

    All the inferotemporal cortices, namely areas 20, 21, part of 36, 37, 38. These cortices support many of the autobiographical records on the basis of which the autobiographical self and extended consciousness can be realized, but they play no role in the proto-self.

  • 3.

    The hippocampus.

  • 4.

    The hippocampal-related cortices, namely areas 28 and 35.

  • 5.

    The prefrontal cortices. Some of these cortices participate in high-level working-memory for spatial, temporal, and language functions. Because of their role in working memory, prefrontal cortices are critical for high levels of extended consciousness, but they play no role in proto-self.

  • 6.

    The cerebellum.

As the brain forms images of an object and of the organism, and as the images of the object affect the state of the organism, yet another level of brain structure creates a nonverbal account of the events that are taking place in the varied brain regions activated as a consequence of the object-organism interaction. The mapping of the organism and the object occurs in first-order neural maps representing proto-self and object, respectively. On the other hand, the account of the causal relationship between object and organism occurs in second-order neural maps. Examples of second-order structures are the cingulate cortices, the thalamus, and the superior colliculi. The subsequent image enhancement is achieved via modulation from basal forebrain/brainstem nuclei, as well as thalamocortical modulation.

The hypothesis thus pivots on the relationship between the changing organism state and the sensorimotor maps of a given object that causes those changes. As the images of the object affect the state of the organism, another level of brain structures creates a nonverbal account of the events that are taking place as a consequence of the object-organism interaction.

In conclusion, the proposal specifies that the essence of consciousness is a continuously generated image of the act of knowing relative to the mental images of the object to be known. The image of knowing is accompanied by an enhancement of the images of the object. And because the image of knowing originates in neural structures fundamentally associated with the representation of body states, the image of knowing is a feeling.

In its normal and optimal operation, core consciousness is the process of achieving an all encompassing imagetic pattern which brings together the pattern for the object, the pattern for the organism, and the pattern for the relationship between the two. The emergence of each of those patterns and their conjoining in time depends on the contributions of individual brain sites working in close cooperation, and the understanding of the mechanisms of consciousness depends on identifying those individual contributions. But the study of such contributions must be considered in the perspective of an important qualification regarding the relation between brain regions and functions: the functions hypothesized here are not located in one brain region or set of regions, but are, rather, a product of the interaction of neural and chemical signals among a set of regions.

Beyond the mechanisms responsible for core consciousness, there are mechanisms responsible for extended consciousness, the protagonist of which is the autobiographical self. Extended consciousness builds on core consciousness, requires memory, and is enhanced by language. The discussion of these mechanisms is outside the scope of this article (but see Damasio, 1999).

The role of brainstem structures in the generation of consciousness is thus a critical one. This article is dedicated to a review of some of the relevant evidence regarding the functional neuroanatomy of the brainstem, an understanding of which is indispensable to the above account of consciousness.

Section snippets

The brainstem and the reticular formation

The brainstem gray matter is organized in nuclei. A brainstem nucleus is a three-dimensional collection of neurons which is usually aligned in parallel to the long axis of the brainstem. Each nucleus has an idiosyncratic cytoarchitecture and tends to have a prevailing neurochemical identity that helps distinguish it from other nuclei; each nucleus has a unique location within the brainstem: each nucleus has connections with a distinct set of other neural structures; and each nucleus tends to

A functional context for the ascending reticular activating system

In the introduction to this article, we noted that it is important to understand the context in which the ascending reticular activating system operates, an issue which includes, among others, the consideration of why the system is located in the brainstem, and of which functional influences drive its operation. A possible answer to such questions can be gleaned in part from the pattern of afferent connections of the brainstem nuclei discussed above. These afferents are grouped based on the

Concluding remarks

The multiple dimensions which describe the overall current state of the organism are mapped in several groups of brainstem nuclei. We believe that this comprehensive and continually changing map of the organism state creates a functional context for the brainstem nuclei whose activity can modulate the operation of rostral brain structures, namely those in the cerebral cortex. In addition, the map of the organism state, along with the fact that such a state is being changed as a result of an

Acknowledgements

Supported in part by a grant from the Mathers Foundation.

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