The Conscious Claustrum
Consciousness and Crick
The definition of consciousness, as a biological phenomenon, remains contested. Language is required in some definitions, while other definitions are based more simply on perceptual awareness of experiences. For the purposes of this article, we will define consciousness as the experience of being aware of our own thoughts and internal state, in response to, and in interaction with, the world around us. Only recently has the study of consciousness been broached by “respectable neuroscientists” where it had previously been confined to the realm of more philosophical disciplines. What can neurobiology tell us about the experience of consciousness?
Francis Crick, who is credited with the discovery of DNA and its function, was a strong advocate of claustrum as the seat of consciousness. Reportedly, Crick’s belief in the importance of this brain structure “bordered on conviction” and he hoped to bring enough attention to the structure to inspire a center devoted to its study. Crick worked on a review on the claustrum on his deathbed with Christof Koch. Why did Francis Crick believe so strongly in the claustrum as the “seat of consciousness”? Perhaps because Crick believed: “In biology, if seeking to understand function, it is usually a good idea to study structure.” The claustrum’s unique structure and connectivity suggest it could be an integrator of sensory experience, potentially giving rise to a unified perception of experience.
The claustrum: The “seat of consciousness”?
The claustrum is a thin, irregular sheet of grey matter on the underside of the neocortex in the center of the brain (located sagitally between external and extreme capsule and mediolaterally between the putamen and insula) with widespread connections throughout the cortex and the rest of the brain. It is present in most mammals but varies significantly between species. In humans, the claustrum is comprised of 3 main cell types: “Type I”, spiny neurons that send projections out of the claustrum and two types of aspiny interneurons, one larger than the other. The interneurons project only within the claustrum and account for only about 10% of the neurons in the claustrum. The claustrum has widespread modality-specific connections across cortex. The modality specific topography in the claustrum arises from projections from “Type I” neurons exclusively to and from the same areas of cortex. Crick and Koch promote the idea that the claustrum could perform what they term “sensory binding”, namely a process of aggregating relevant information to develop a single, uniform experience. They suggest that this makes the claustrum an attractive candidate structure for the “seat of consciousness”.
“Binding” and Integration: The evidence
The claustrum is buried deep inside the cortex and differs across species. In light of this, the claustrum is difficult to study, but researchers continue to pursue an understanding of this brain area using experimental and computational methods. A recent electrophysiological study recorded from neurons in the claustrum of monkeys and demonstrated that pyramidal (like “Type I”) neurons in this area respond to only one sensory modality. While their technique and ability to record from this hard to reach area is laudable, their analysis is somewhat lacking, in that they exclude the effects of the interneuron population as a potential source of integration across modalities, even in light of its widespread connectivity throughout the claustrum.
Other studies have focused on the potential power of this same interneuron population (a small percentage of the total number of neurons in this area) and proposed computational methods by which the claustrum might be capable of achieving the kind of integration Crick proposed as the foundation of conscious experience. John Smythies at UCSD suggested neurons in the claustrum form an ‘AND’ gate. In his proposed model, each interneuron is activated by one visual attribute (e.g. red vrs square), while the pyramidal cell fires in response to both attributes (red AND square). Because the interneuron is activated only by one attribute, successive inputs coding “red” in the absence of “square” sufficiently activate the interneuron to inhibit the pyramidal cell firing in response to just “red”. In this proposed model, the interneuron prevents against encoding a coincidence that is not present.
Smythies updated this hypothesis in a review paper with authors Edelstein and Ramachandran. Here the authors proposed that the claustrum acts not as coincidence detector at the single neuron level, but as a detector of synchrony across various parts of the brain. They suggest a role for gamma frequency oscillations in discriminating “match” and “non-match” activity patterns across the cortex and describe how the rich interconnected interneurons in the claustrum could synchronize disparate parts of the cortex.
The integrated sensory experience
The claustrum is rich in kappa opioid receptors, which are expressed in a number of brain regions, but most densely in the claustrum. These receptors are activated by compounds in the hallucinogenic drug salvia. People taking salvia report “intense sensory synesthesia in which subjects claim that they see sounds and hear sights”. Kappa opiod receptor activation is believed to cause a presynaptic inhibition of GABA release. This change in inhibitory signaling may be responsible for the altered state of consciousness induced by salvia, and could provide further evidence for the role of inhibition in the claustrum in creating a unified perceptual experience.
The claustrum has been implicated in other experiences, such as orgasm, that involve integration of various sensory experiences, and REM sleep, during which “conscious” experience is often nonsensical. The strangeness of dream consciousness could arise from firing of the neurons of the claustrum in patterns not present during waking perception, which drive, or are driven by, interactions with the cortex.
Conclusions: The importance of inhibition
The mechanisms by which the claustrum computes, “integrates” and influences the rest of brain remain poorly understood. Due to the diversity of the claustrum across species, it is challenging to study the neurobiological origins of human consciousness using animal models. Data from the treatment of epileptic patients in a clinical setting (patients have experienced “loss of consciousness” when stimulation is given to the claustrum), and from salvia users are currently the best available for studying the role of claustrum in human consciousness. In spite of the limited data, many models and hypotheses have been made and examined regarding the purpose of the claustrum, and much attention has been given to Crick’s theory on consciousness. From the recent evidence presented here, it seems likely that the interneuron population in the claustrum is largely responsible for the ability of the claustrum to integrate across sensory modalities, if it indeed does. The neurobiology community would be well served to follow Crick’s advice about the link between structure and function. Understanding the computations of interneurons in the claustrum, and more importantly, their interactions with “Type I” neurons and the cortex at large, would yield great insights into the function of the claustrum, and shed light on the validity of Crick’s convictions about this puzzling piece of cortex, and its potential to serve as the “seat of consciousness”.