Seeing Consciousness Through the Lens of Memory

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infected rhesus macaques. bioRxiv https://doi. what the experience is about, for org/10.1101/2020.03.13.990226. My Word 17. McCray Jr., P.B., Pewe, L., Wohlford-Lenane, C., example, an apple or a snake. Hickey, M., Manzel, L., Shi, L., Netland, J., Seeing First-order theories, such as Jia, H.P., Halabi, C., Sigmund, C.D., et al. recurrent processing theory [2,3], posit (2007). Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome consciousness that consciousness originates in brain coronavirus. J. Virol. 81, 813–821. regions specialized in the processing 18. Docherty, A.B., Harrison, E.M., Green, C.A., through the lens of Hardwick, H.E., Pius, R., Norman, L., of a given kind of information. For Holden, K.A., Read, J.M., Dondelinger, F., memory perceptual states of consciousness, Carson, G., et al. (2020). Features of 20,133 these include, for instance, visual UK patients in hospital with covid-19 using the ISARIC WHO Clinical Characterisation Protocol: or auditory cortices. For emotions prospective observational cohort study. BMJ Joseph E. LeDoux1,2,3,* like fear, subcortical areas such as 369, m1985. and Hakwan Lau4,5 19. Mao, L., Jin, H., Wang, M., Hu, Y., Chen, S., the amygdala have been proposed He, Q., Chang, J., Hong, C., Zhou, Y., Wang, D., to be a fi rst-order locus [4]. In fi rst- et al. (2020). Neurologic manifestations of We humans have long thought of order theories, the phenomenal feel hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 77, 1–9. ourselves in terms of bodily and mental and content of the experience are 20. Poyiadji, N., Shahin, G., Noujaim, D., Stone, M., spheres of existence. These days fully accounted for by some specifi c Patel, S., and Griffi th, B. (2020). COVID-19- associated acute hemorrhagic necrotizing many of us understand that the mental pattern of neural activity within these encephalopathy: CT and MRI features. 296, aspect of who we are is embedded fi rst-order areas. E119–E120. in the part of the body known as the Higher-order theories, on the 21. Klok, F.A., Kruip, M., van der Meer, N.J.M., Arbous, M.S., Gommers, D., Kant, K.M., Kaptein, brain, and is therefore also part of our other hand, suggest that fi rst- F.H.J., van Paassen, J., Stals, M.A.M., Huisman, physical, bodily self. Although most order representations may not be M.V., et al. (2020). Incidence of thrombotic complications in critically ill ICU patients with of us accept this scientifi c conclusion suffi cient to account for either the COVID-19. Thromb. Res. 191, 145–147. about the physicality of the mind, phenomenal feel or the content of many nevertheless feel as though the conscious experience [5–7]. They 1Radboud University, 6525 XZ Nijmegen, their mind possesses some quality posit that some higher-order cognitive The Netherlands. 2University Medical Center, lacking in other physical systems mechanism, possibly involving circuits Utrecht Brain Center, Utrecht University, 3584 within their body, and even within their in prefrontal cortex, is needed in order 3 CG Utrecht, The Netherlands. Netherlands brain — we have fi rst-hand knowledge to monitor or meta-represent the Cancer Institute, 1066 CX Amsterdam, The Netherlands. 4Radboud University Medical of our thoughts and feelings, but not fi rst-order information. As such, the Center, 6525 GA Nijmegen, The Netherlands. of the neural processes that control information represented in fi rst-order 5Maastricht University, 6211 LK Maastricht, body processes related to digestion, structures remains non-conscious The Netherlands. 6University of Groningen, respiration, heart rhythm, and so on, (or pre-conscious) if no higher-order 9712 CP Groningen, The Netherlands. nor of the brain’s control of much of re-representation is involved. With 7 University of Groningen, University our behavior. respect to fear, this view posits Medical Center, 9713 GZ Groningen, The Netherlands. 8Biomedical Primate Research In this My Word, we explore the that the amygdala controls non- Center, 2288 GJ Rijswijk, The Netherlands. question of what is different about conscious defensive responses, 9Metris BV, 2132 NG Hoofddorp, The a brain state about which you are such as behavioral and physiological Netherlands. 10University Medical Center, conscious from one that you are responses to threats, but that higher- 3584 CX Utrecht, The Netherlands. 11Leiden not? We will argue that all conscious order re-representation, possibly University Medical Center, 2333 ZA Leiden, experiences involve elements of involving prefrontal cortex, is required The Netherlands. 12Amsterdam University Medical Centers, 1105 AZ Amsterdam, memory and meta-representation. in order to generate the subjective The Netherlands. 13Erasmus University This framework may help us better experience of fear in response to the Medical Center, 3015 GD Rotterdam, The understand the subjective qualitative threatening stimulus [7–9]. For higher- Netherlands. 14Netherlands Institute for character of conscious experiences, order theories, the phenomenal quality Neuroscience, Royal Netherlands Academy as well as why meta-representations and conscious content both require of Arts and Sciences, 1105 BA Amsterdam, may be involved in generating even the higher-order state. The Netherlands. 15Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 the simplest of such experiences. XH Amsterdam, The Netherlands. 16Charles Memory and consciousness River, 5231 DD Den Bosch, The Netherlands. Phenomenal ‘feel’ and conscious The pioneering 19th century 17Oncode Institute, 3521 AL Utrecht, The content psychologist Hermann von Helmholtz Netherlands. 18Wageningen University, William James famously referred to the proposed that conscious perception 6708 PB Wageningen, The Netherlands. special property of conscious states is an ‘unconscious inference’ based in 19Utrecht University, 3512 JE Utrecht, The Netherlands. 20Life and Medical Sciences in terms of ‘warmth and intimacy’. part on memory. Consistent with von Institute, University of Bonn, 53115 Bonn, These days it is common to describe Helmholtz’s logic, we propose that Germany. 21Netherlands Institute of Ecology, this as a phenomenal ‘feeling’ — the all states of consciousness depend Wageningen University, 6708 PB Wageningen, quality that makes red seem red, an on memory [7–9], and specifi cally The Netherlands. 22Viroclinics Xplore, 5374 apple seem like an apple, and fear on mechanisms that integrate 23 RE Schaijk, The Netherlands. Wageningen feel fearful [1]. There is considerable sensory and memory information Bioveterinary Research, 8221 RA Lelystad, The Netherlands. disagreement about what this quality unconsciously (i.e. pre-consciously). *E-mail: [email protected]; is and how it may come about in the A fundamental distinction in [email protected] brain in relation to the actual content; memory research is between

Table 1. Anoetic, noetic, and autonoetic consciousness. Consciousness Knowledge Memory Meta-representation Self Example thought

Anoetic Non-knowing Procedural Non-cognitive Implicit Thought not involved

Noetic Fact-knowing Semantic Cognitive Assumed “There is an apple”

Autonoetic Self-knowing Episodic Cognitive Explicit “I see an apple” memories that are formed and stored Noetic states of consciousness relations between dynamical neural in a way that can be consciously depend on semantic memories of profi les and sensory inputs. These retrieved, and memories that are factual and conceptual information implicit memories are used to classify stored implicitly, and hence are about what things are and are not. the wavelength of the present stimulus not consciously experienced when For example, seeing a bird and with other stimuli from the past retrieved [10]. People can have recognizing it as a robin not only with similar neural profi les. Indeed, conscious introspections and talk requires sensory processing of the empirical fi ndings show that colors about explicit memories, but they visual properties of the present and other low-level visual features can only show the effects of past robin, but also semantic, including are embedded in a local spatial and implicit procedural learning through conceptual, memories about what temporal contexts of other neurons nonverbal behavior. One consequence birds and robins are. In sharp contrast and are processed relative to these is that a person with damage to to autonoesis, noetic states do not [14]. The color of a stimulus, when the circuits underlying explicit require explicit self-awareness and do not conceptualized by semantic memories can procedurally acquire not support mental time travel. memory, can only be experienced and perform behaviors which they A third kind of state recognized relationally with respect to other have no conscious memory of having by Tulving is anoetic awareness. possible color representations, which acquired; conversely, damage to Although the most basic, it is the is what accumulated procedural one of the many procedural memory least intuitive, and requires some memories offer. Accordingly, what we circuits prevents behavioral learning discussion. Tulving referred to anoetic consciously see as red only looks red by that system, but spares the ability consciousness as states of ‘non- because of the way it looks similar to to remember the episode in which knowing’, by which he meant that and different from other stimuli that they tried to learn the behavioral these do not themselves directly rely have been seen in the past [13,14]. response. on or contribute to our conceptual, To illustrate the relationship between An infl uential view of the relation explicit knowledge, and hence are these three kinds of conscious states, between memory and consciousness not readily available for introspection. consider the experience of seeing a red was developed by Endel Tulving [11]. They are conceptually similar to apple (Figure 1). An anoetic experience He identifi ed three kinds of conscious what fi rst-order theorists refer to as of ‘redness’, lacking the conceptual states that are each associated with ‘phenomenal consciousness’ [2,3], support of semantic memory, remains a distinct kind of memory (Table 1). and have also been described as as a sensation of some complex set Although Tulving’s taxonomy was ‘non-refl ective qualia’ that occur in of wavelengths classifi ed in relation proposed to account for how memory primitive emotional states related to to past experiences with similar contributes to consciousness, we survival behaviors involving defense, wavelengths stored via procedural believe it is also useful as a way of mating, feeding and so on [4]. They memories. With semantic memory, the using memory to partition conscious exist on the ‘fringe’ or ‘penumbra’ of wavelengths become noetic states in states and thereby better understand consciousness, to borrow expressions which you are informed by what you consciousness itself. from William James. conceptually understand ‘red’ to be, Autonoetic consciousness is Although Tulving and others and how red relates to other features, explicitly about your self in the describe anoetic states as temporally such as shape, allowing an awareness present moment in relation to your and spatially bound to the current that a red apple is present. If your past and future. It is grounded in moment, and mainly about the self, via episodic memory, is explicitly episodic memories: memories about here and now, we believe this brought into the experience, an experiences you have had. The needs qualifi cation. This is true of autonoetic state of a red apple exists, episodic record of your life provides a the sensory component of such perhaps involving the recollection of sense of continuity with your personal states — but the involvement of some experience involving apples from past (recollecting seeing a robin on a implicit, procedural memories gives your past, or anticipating an experience certain day and in a particular place); the moment a connection to relevant in your future. it also allows one to project into aspects of one’s implicit history possible personal futures (wondering with similar stimuli [11–13]. For Meta-representations and what kinds of birds you might see on example, through past exposures consciousness your next outing). This ability to visit to wavelengths within a certain Each of Tulving’s three conscious your personal past and hypothetical range, the visual cortex, via synaptic states have been said to be based on future is called mental time travel [11]. plasticity, has implicitly learned a pre-conscious meta-representation

Current Biology 30, R1009–R1035, September 21, 2020 R1019 ll Magazine

over time, including our past, and our Conscious Anoetic Noetic Autonoetic possible future, selves. state consciousness consciousness consciousness In summary, the three kinds of meta-representations seem to AAnoeticnoetic NNoeticoetic Autonoetic narnarrationration narnarrationration narration serve the same purpose — they Schema Procedural ConceptualCon Self appear to function as higher-order schema scschema schema re-representations of lower-order sensory and memory information. If correct, the implication is that Meta- Pre-consciousonscious Pre-consciousonscious Pre-consciouson anoeticoetic noeticoetic autonoeticono all conscious experiences are representation Meta-representationpresentation Meta-representationresentation Meta-representationpre preceded by a non-conscious meta- representation, without which there is no consciousness. We suggest that these meta-representations involve areas of prefrontal cortex, possibly Lower-order Sensoryry input + Semanticmantic Episodic state proceduralral memory memory memory including dorsal and ventral lateral prefrontal cortex, the frontal pole, and medial frontal areas [6–9,15–17]. Next, we consider how these pre-conscious External meta-representations might be stimulus translated into conscious content.

Current Biology The stories we tell ourselves Figure 1. Meta-representations, narrations, schema, and consciousness. Novelists, inspired by William The model developed in this paper involves three key ideas. First, conscious experiences of James’ description of ‘the stream of events in the world involve lower-order elements of memory that are meta-represented and ﬁ l- consciousness’, have capitalized on tered by schemata that narrate the content of the conscious experience. Second, the lower-order the narrative, story-like quality of the state, meta-representation, schema, narrative, and content differ for anoetic, noetic, and auto- human mind. Scientists, too, have noetic experiences. Third, the states are hierarchical, such that the implicit procedural memory element of anoetic consciousness is passed on to noetic and autonoetic states, providing these followed this lead [18–20], noting that explicit conscious experiences with a ‘phenomenal feel’ and sense of ownership. one’s self has a narrative-like structure that gives us psychological coherence over time. This coherence is probably [12]. As such, Tulving’s model can For this to happen, some additional maintained by perpetual revisions, be thought of as a kind of higher- mechanisms may have to implicitly with the results carried forward though order theory in which conscious retrieve, perhaps via an implicit memory. For example, if a new noetic awareness arises from the re- schema (see below), the dynamical or autonoetic experience is discordant representation of a lower-order state profiles of early sensory activity, in with stored semantic or episodic by a higher-order one [5–9,12]. In order to draw the correct perceptual memories, either the anomaly has to other words, as in higher-order theory, inference. In this sense, we propose be accepted or the stored knowledge the meta-representations are pre- that meta-representations contribute has to be updated. Although the term conscious antecedents to conscious to even the simplest perception of ‘narrative’, when used in relation to experiences. non-conceptualized redness [6,7,12]. mental states, most commonly refers In the case of anoetic Noetic experiences add semantic to a verbal story line told by our inner consciousness, the lower-order knowledge stored in medial and voice, our conscious experiences can state is not simply a pure sensory lateral cortical areas of the temporal be visual or even multimodal, and the state of visual cortex, as claimed by lobe [8,10] to the anoetic state. This underlying narratives, in turn, would lower-order theories. It is, as noted, a creates conceptualized perceptual be as well. representation in which raw sensory content about what the stimulus is, A common assumption is that input has been compared with and how it relates to the present narrations are outcomes of conscious implicit procedural memories from situation. If you have the conscious states — they occur post-consciously. similar past visual experiences. In thought that you are seeing the But we propose that narratives are further contrast to first-order theories, redness of an apple it is because you also involved in the initial generation of we suggest that even an anoetic, are noetically experiencing the content the content of noetic and autonoetic non-reflective, conscious experience of the meta-representation. consciousness. In particular, we of red depends on processing beyond For autonoetic states, episodic suggest narratives reﬂ ect the complex visual cortex. For example, in order memories about relevant past memory processes known as schema to experience red as being about a personal experiences stored in the [8,21]. These are collections of stimulus in the world the brain must temporal lobe are added to the noetic semantic memories about recurring distinguish it from other kinds of state. Through the mental time-travel objects and situations that serve as visual cortex states based on internal feature of episodic memory, we feel non-conscious conceptual templates visual imagery or neural noise [15]. consciously connected to our self for storing new memories and for

R1020 Current Biology 30, R1009–R1035, September 21, 2020 ll Magazine understanding present situations in Now consider this idea in the ability to understand the emotional relation to one’s needs and goals context of a complex real-life situation lives of others is the fact that emotion [7–9,21]. Of interest is that the ventral in which you are not just seeing a schema, and hence emotional medial prefrontal cortex has a role in stimulus but are in a life-threatening experiences, differ not only between both schema [8,21] and narrations encounter with a dangerous stimulus individuals, but also between social [22]. This area interconnects with such as a rattlesnake. Sensory and cultural groups [27,28]. other prefrontal areas that have information about the snake will not By contrast with other proposals been implicated in metacognition simply be transmitted from visual about the role of anoetic states and consciousness, such as the cortex areas to memory and higher in phenomenal experience, our dorsal lateral frontal cortex and the cognitive circuits. It will also be view differs in two key respects. frontal pole [6–9,15–17,23,24]. We transmitted to subcortical circuits, In our model, fi rst-order neural hypothesize that when the relevant such as those involving the amygdala, activity is not all there is to anoetic prefrontal circuitry is damaged, pre- that organize defensive behaviors consciousness. Thus, we maintain conscious narrations and the contents and physiological reactions, and that the phenomenal feel of visual of conscious experiences should be that also activate arousal systems. consciousness is not simply a affected. The behavioral and physiological state of visual cortex [2,3], and the responses also produce sensory and phenomenal feel of fear is neither Owning up chemical signals that are represented an amygdala state [4] nor a state The preceding discussion begs the in the brain as body states [4,8,9,26]. representing body sensations [26]. question of how anoetic states fi t Importantly, these circuits have also Only once lower-order states are meta- into our narrative framework of noetic acquired procedural memories about represented does anoetic phenomenal and autonoetic consciousness. We the relevant neural responses made consciousness result. Second, we suggest that anoetic states may play a in the past. These will determine, for suggest in any real-world experience, crucial role in the feeling of ownership example, how the present degree of many other procedural brain systems we have about our mental states. activation of amygdala, arousal, or will also be implicitly activated, Mental state ownership is so natural body state circuits match levels from besides the obvious ones mentioned and automatic that we never have to the past. Still other implicit circuits above, and all will contribute to the explicitly affi rm it. This fact is put into are also likely activated. For example, phenomenal feel, the familiarity, of the stark relief by certain neurological or object recognition or auditory mental moment, when monitored by psychiatric conditions in which people pattern recognition circuits might be the meta-representation. lose the sense that their thoughts primed to detect related stimuli, and The philosopher Owen Flanagan and feelings belong to them [25]. A motor circuits primed to respond [29] noted that theories about the self common view is that this personal behaviorally. overrate the role of autobiographical relationship to mental states is due All of these implicit states will memories, and underestimate the role to autobiographical memory, which become part of an anoetic background of the much larger class of events that includes episodic and semantic monitored by the meta-representation are experienced but not remembered. memories about our self. Certainly, our that also includes semantic conceptual We broadly agree but suggest that autobiographical memories, especially content about snakes and episodic the reason these experiences may episodic ones, are important in giving content about your personal contribute is because they are us a sense of continuity over time. But experiences with snakes. The content implicitly remembered via procedural there may be more to the sense of of the meta-representation as a whole, memory. ownership than that. we suggest, will be schematized As noted, prefrontal circuits As we noted, procedural memories (implicitly by procedural memory and have been implicated in subjective give anoetic states a connection to explicitly by semantic memory) and metacognition, narratives, schemata, implicit aspects of one’s history that narrated [27] (Figure 1). Hence you consciousness, including self- are relevant to the present stimulus will fi nd yourself in the autonoetic consciousness and emotional situation. The fringe or penumbral state of fear [8,9,27], without having consciousness [6–9,15,16,17,23,24,27], quality of these goes unnoticed to explicitly infer that fear is what but also in the ownership of mental because anoetic states are often you are feeling. You know it is fear states [25], and in the ‘feeling of embedded in noetic and/or autonoetic because you know what fear feels rightness’, ‘feeling of knowing’, and states with actual conscious content like to you. Other people do not have ‘feeling of familiarity’ of such states [4]. It is mainly in laboratory studies your fi rst-hand procedural memories [21,25]. Perhaps a general purpose where explicit consciousness of your neurophysiological responses higher-cognitive prefrontal network involvement is minimized that a pure to threats that accompany your might underlie all kinds of conscious anoetic experience can be isolated. But autonoetic states of fear narrated by experiences [5–9,27]. in a real-life situation the procedural your schema. That’s why emotions are memories, and their implicit connection personal — only you can have your Reconciling fi rst-order and higher- to your past, may be what makes a emotions [8,9,27]. But through shared order theories noetic or autonoetic state feel it is, by vocabulary, we can extrapolate and The above provides a possible mere acquaintance [25], yours without infer what others might feel in similar rapprochement between the fi rst- you ever having to explicitly affi rm that. situations [8,27]. Complicating our order and higher-order theories of

Current Biology 30, R1009–R1035, September 21, 2020 R1021 ll Magazine consciousness. First-order theorists speculate on consciousness for Brandl, J. Perner, and J. Proust, eds. (Oxford: Oxford University Press), pp. 289–301. have claimed that phenomenal sheer intellectual challenge. But our 13. Clark, A. (2000). A Theory of Sentience (New consciousness is theirs alone, and intentions are actually practical: we York: Oxford University Press). that higher-order theory is only about believe that progress in psychiatry and 14. Schwartz, O., Hsu, A., and Dayan, P. (2007). Space and time in visual context. Nat. Rev. cognitive access and interpretation clinical psychology has been impeded Neurosci. 8, 522–535. of the experiences. For them higher- by the fact that these fi elds have 15. Lau, H. (2019). Consciousness, metacognition, & perceptual reality monitoring. 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R1022 Current Biology 30, R1009–R1035, September 21, 2020