With sad fondness, I post the email conversation I had with the late Dr. Behrendt.
When the EMMOSE idea occurred to me in 2013, I started exploring the literature, to find who had already started publishing. I found the late Gerald Edelman's book "The Remembered Present", which demonstrated that the hippocampus had the requisite 're-entrant' anatomy which would allow for buffering and binding of information into an experience.
But the only actual model that I could find belonged to Ralf-Peter Behrendt. He was a German-born psychiatrist, working in the UK, especially with aging and schizophrenic patients. In 2010, he published (what I think is) his first paper linking consciousness to the hippocampus. And in 2013, he published a working anatomical model, which is the first paper of his I found.
We began our conversation in 2013, and continued it until 2018, when I stopped hearing back from him. I was afraid I had said something wrong; offended him. It wasn't until 2021 that I found a death notice. I was always hoping to meet Ralf in person, and of course to interview him for the film. But also, I was sad because I felt I had lost a brother. We saw this problem the same way, and that connected us, across our differences.
We absolutely did have differences about our respective models, which will play out in the conversation below. We even both published journal responses to each other, which I'll attach at the end.
Those theoretical differences led me to feel I had to publish my paper, as well. There were elements (like the perception of mind and body) which I felt needed to be directly addressed. I hope that, despite some differences, Ralf's model and mine can be read as complementary literature. At least we agree on the pre-hippocampal story.
Of course, I am posting these emails without Ralf's permission, my apologies. But I don't think there's anything in here that would embarrass him in any way. I'm sure he would've been fine with this. If I'm wrong, then I owe you one, Ralf.
Dear Dr. Behrendt,
I've just finished reading "Conscious Experience and Episodic Memory: Hippocampus at the Crossroads", and I think it's brilliant!
What you are describing fits, without exception, all of the examples of conscious experience that I have heard of, and I believe it dovetails very well with many of the great mysteries of subjectivity, like "driving mind", confabulation, hallucination, the 'self' as a construct, dissociative identity disorder, flashbacks, blindsight, Libet's timing experiments, even hemispatial neglect and anosognosia. These are the mysteries that any theory on consciousness has to answer, and I think you've done it!
I am producing a documentary-in-progress on consciousness, and would love to interview you for it. I am planning on being in Tucson, AZ, USA this April for the TSC conference, to conduct a few remaining interviews, before I try to finish editing the film. I don't know if you are thinking of attending, but if you are, I'd really appreciate an hour-90 minutes of your time, while you are there, to talk about the hippocampus' role.
If you are not attending that TSC conference, then perhaps we can find another opportunity to meet. If you have any business in the states, soon, especially if you're traveling anywhere near Los Angeles, where I live, I'd very much like to interview you at that point. Or perhaps I can come to you (although the documentary is self-funded, at this point, so it's difficult to make large expenditures).
This film is a collaboration between consciousness researcher Bill Faw and me, his filmmaking son.
Thank you for considering this request!
Matt Faw, filmmaker
Dear Matt Faw
thank you for your positive feedback. I have to say that I am surprised that despite the prominence of the problem of consciousness in neuroscience, very little attention has been paid to the hippocampus. I agree, it all fits together, but most people will find it difficult to shift away from their preconceived notion that, because consciousness is the seemingly greatest achievement of the evolution of the nervous system, it has to be located in or subserved by the neocortex. It's a bit like having to accept that the earth is not in the middle of the universe :)
I am afraid that I have no plans coming to the US in the near future. I work as a full time psychiatrist and I need to go back to Germany during my annual leave periods to support and be with my mother (I'm her only child).
Let me know if you coming to Europe at some point, but I have to say the idea of an interview causes me some anxiety and I would find it very stressful to be filmed. I am flattered by your suggestion anyway, so thank you very much!
Ralf
Thank you so much for your quick response, Ralf. Too bad I won't see you in Tucson. I'm going to start looking for opportunities to come to the UK.
I understand if the filming is anxiety-producing, but the good thing is, it'll be completely edited, so you can always back up and start a sentence over, take your time think about answers, etc. There will be no pressure, during the interview, to perform.
As far as the hippocampus goes, I've seen Christoph Koch dismiss it as a possibility, because of H.M. Because he was "conscious", therefore the hippocampus wasn't the seat of consciousness. But I think that just shows that consciousness is not actually the animating or intelligent force; it's just memory, the product of the hippocampus. All of the real intelligence of the organism happens prior to memory (well, that's saying it too strongly, since so much associative work actually happens in the hippocampus). But at least it suggests that the "I" at the center of subjective experience is not the decider or the perceiver; it's just a construct for memory. "I" have been assembled, after the fact, in order to give context to my memories, cobbled together from self-data throughout the brain. "I" do not have access to perceptions; rather "I" and perceptions are generated together as part of the multimodal movie.
All those activities that happen at the hippocampus, like daydreaming, spatial manipulation, pre-visualization, recall, all feel like "I" am doing them. And all those things that happen prior to the hippocampus, like recognizing the meaning of the words on this screen, all seem "automatic", because they are not represented in memory, but those processes are truly intelligent, not zombie or "unconscious". It is the "I" which is the illusion, the "conscious process" which is the illusion. As I see it, there are pre-memory processes, and there is memory. And our entire experience exists in the latter.
I think that's part of what's so tough about accepting the hippocampus as the seat of subjective experience; it implies that "I" am just a memory, when I so desperately want to be the intelligence.
But it also makes total sense in things like "driving mind", which has always been explained as automaticity, even though I think that's an absurd explanation. Of course the brain didn't do it on automatic; the exact same "driving modules" did the driving, as always (all of which are in the task-positive network). It's just that the hippocampus was so pre-occupied by the default network in a daydream, that the flow of data from the task-positive network was excluded from being formed into memory. I "wake up" (meaning the daydream ends, and the task-positive data flows back in), and then realize that I have no memory of the drive. But that just shows that "I" and "conscious awareness" are just memory, not the driver.
And so on... I see applications of this theory in hemispatial neglect, blindsight, anosognosia, etc. And if a theory fits well with all the major mysteries of subjectivity, that's a pretty good sign!
Thanks again for your reply, Ralf. It will take me some time to get over to Europe, for money reasons, but I look forward to meeting you before too long. In the meantime, I'd love to continue this conversation with you further, look deeper into the implications of the theory, since I plan to make it the crux of my documentary.
with much respect,
Matt Faw
Dear Matt,
I agree with almost all of what you said: consciousness is episodic memory formation in action, and whatever is assembled in this contextualized, allocentric image (memory) of the world is preprocessed in the neocortex. I would only have a slight objection regarding the notion of 'I' and consciousness being equivalent. The 'I' is just an aspect of the complex episodic memory that is formed at any one time (and of course the 'I' has nothing to do with agency), one however that is an essential part only of memories formed in any social (real or imaginary) context: it is that aspect of the memory formed and the situation comprehended that reflects one's acceptance by the social surround, or one's potential to be appraised etc.; there are clear evolutionary reasons for this (and I'm writing a book about this, from perspective of psychoanalysis). The 'I' is a part of the reflection or rather simulation of the world and as such it assists assessment of the social situation in which one finds oneself, and hence helps to regulate the overall emotional response of the organism to this situation. The self helps social orientation (and thereby provides a situational context for individual - essentially unconscious - social actions), much as landmarks helps self-localization of the organism on a map.
Did Dr Koch see my paper by any chance? Regarding HM, the hippocampus was not actually completely destroyed and, you are absolutely right, his rejection of the hippocampus as the 'site of consciousness' hinges on the notion that consciousness plays an essential role in behaviour, which it does not as you rightly pointed out. It does play some role though, the same role played by episodic memory (and nobody can claim that episodic or declarative memory plays no role).
It would be good indeed to see you sometime. I didn't know there is somebody out there who is receptive to the position I argued. It is refreshing to know that there is! :)
Ralf
Dear Ralf,
Thanks so much for your reply. I'm afraid I can't speak as to whether Dr. Koch has seen your paper; I was just reading an older article he had written, in which he momentarily entertained the idea of the hippocampus as the center of consciousness, and then used H.M. to dismiss that possibility. However, Antonio Damasio, who worked with complete bilateral damage hippocampal patient Daniel, makes it clear in "The Feeling of What Happens" that Daniel does not have the kind of phenomenal "consciousness" that someone with access to episodic memories would have. So I see H.M. and Daniel as having Actual Experience and Interaction with the world, but never having a subjective experience representation of that, for memory.
I also think that Daniel Dennett's "Cartesian Theater" argument has scared a lot of people off of the idea of subjective experience as a multimodal movie. But his argument really shows the absurdity of an inner me, and doesn't get rid of the evidence for experience-as-construction. If the "me" is part of the construct, then there is no infinite regress of homunculi.
I absolutely agree with you that episodic memory and the self still do play important causal roles in the life of the mind, as H.M. and Daniel demonstrate.
After all, memory defines reality, quite literally so with veterans who experience flashbacks. Sufferers of dissociative identity disorder have their memories segmented off from each other. Since the 'I' is generated within memory, each memory stream has its own 'I'.
As you point out, schizophrenics receive confused and redundant data for creating their simulations, and the result is a very messy reality. In fact, I think schizophrenics may point to why most brain data is left out of the simulation: because to have our memories cluttered with multiple interpretations and background processing would create a reality that was nearly impossible to navigate.
Hemispatial neglect shows that when incomplete data arrives at the hippocampus, the simulator does its best to make a reality out of it, anyway. Likewise, a patient with Capgras syndrome builds his memory simulation with certain emotional data missing, so when mom is simulated, she looks and sounds like mom, but does not feel like her. It is actually more appealing to come up with the preposterous notion that mom is an impostor, then it is to doubt one's own reality simulation. That's powerful.
Confabulation is another interesting case. Patients with frontal lobe amnesia (as I'm sure you've experienced) can create a memory-like simulation out of whatever data is available, but patients with complete bilateral hippocampal damage do not confabulate. They cannot construct memories, and so they cannot mis-construct them, either.
And on and on. I see tons of evidence pointing in the direction of your theory. The fact that the visual cortices do not construct an entire scene, but rely on the parahippocampal gyrus to construct it, and the hippocampus to bind the objects, scene and self-information. The fact that prospection, imagination, mental navigation, episodic recall and even theory of mind all display similar neural patterns of the default network activating the hippocampus, implying that the hippocampus is the "mind's eye" for the default network. In particular, this line of research seems to implicate the vmPFC in some very powerful self-processing, in connection with the hippocampus as its "workspace", to use Baar's term.
Really amazing stuff, and I'm so happy to be making this documentary now, to be able to feature this cutting-edge science and theory. Of course, I know that most of the scientific community has not yet grasped what you are proposing, but I am confident that that will happen soon.
with much respect,
matt faw
Dear Matt
What you say about Damasio's patient Daniel is very interesting. The way i would phrase the argument about hallucinations and dreaming is that the autoassociation network's settling at each phase of the theta rhythm on stable states (which reflect the formation of event memories) is not sufficiently constrained by input from the neocortex via the entorhinal cortex, and there is some physiological evidence (from animal experiments) to support this, as referenced in my paper. This lack of constrainment of attractor dynamics is due to lack of inhibitory activity in the hippocampus in schizophrenia. Obviously one can also hallucinate or have maladaptive conscious experience if the neocortical input to the hippocampus itself is underconstrained by what happens in external physical reality. But I agree it is in any case the binding together of multimodal information and its embedding in an allocentric context in the hippocampus that generates conscious experience. The visual cortex as you rightly pointed out does not have the connectivity or the inputs to do this and does not represent information allocentrically (with reference to an external framework) anyway.
Regarding the 'me' or 'I', i think this is not a necessary part of conscious experience, but whenever you think about consciousness or monitor your thoughts it will be there, because on some remote level such thinking or monitoring is relevant to the social self, relevant to what we want to achieve in the social world etc. There is no risk of homuncular fallacy if we recognize that the 'I' is merely an abstract aspect of the reflected or simulated image of the world, similar to trees and similarly also to emotional feelings. And it can be shown from the point of view of psychoanalytic theory that 'I' is an aspect of emotional experience that embeds the simulation of the world, it is intimately linked with feelings of safety versus anxiety, feelings that critically socially determined in humans. The most exciting aspect of the view of the hippocampus as a simulator and mapping device (mapping allocentric information onto some abstract map or space, including social space) is the implications it has for our understanding of emotions....
Kind regards
Ralf
Thank you so much for your response, Ralf! I am intensely interested in this topic, so to receive your correspondence is extremely valuable to me.
I agree the 'I' is not a necessary part of consciousness, and the more deeply involved we are in our engagement with the outside world (task-positive network), the less self seems to be involved. But self comes up especially in lying-in-bed rumination: what did I do today, and how do I feel about it? And it comes up in self-consciousness during social experience: how am I perceived? Am I doing the right thing? There is something about the loops that self-reflection creates, which solidifies the sense of self, makes it into an entity.
What you wrote about hallucination reminds me of one of the interviews I've conducted, with the British researcher Robin Cartright-Harris, who is studying the effects of psilocybin on the brain. His finding was that psilocybin dramatically decreased the activation of various hubs of the brain, decreasing inter-modular interaction, and allowing each module more latitude in coming up with its interpretations of internal and external stimuli. He talked about psychedelic hallucinations as the brain making wrong predictions, as to what the incoming stimulus meant.
https://vimeo.com/44412867
That's one of the most exciting aspects of hippocampal simulation, to me: the idea that we are each generating our own reality, but that we assume that everyone else lives in the same reality that do. For example, the most absolutely certain people in the world (fundamentalists, jihadis, extremists) are also the most obnoxious, because they have such rigid constructs, and are always trying to force others to live by their imagined rules. For me, the simulation of experience points to how easily belief is represented as if it is "knowledge", the simulation as if it is real.
You mentioned that the most exciting aspect to you was in our understanding of emotions. I'm very curious about this. Can you say more?
Sincerely,
matt faw
Dear Matt,
emotions are a facet of the simulated world. Conscious experiences and declarative memories map onto emotional feelings like landmarks map onto locations. Just like the sense of location provides us with an overarching framework for our actions in the world, so do emotions. I'm talking about emotional feelings (as opposed to affective states, which have autonomic and other components) and how they link into modes of behaviour via the anterior hippocampus-medial prefrontal cortex axis. I wrote an article about that, but it's not as easy to read as the Frontiers one (I can send you a pdf if you wish). The beautiful point is this: the world around us - being simply a simulation, as you appreciate - is a world constituted of objects and events (simulated ones) that are embedded not only in a visuospatial context but in an emotional context as well. Emotions and our experience of the world are not separable; emotions are an integral part of the world as we experience it. Only when making the 'mistake' of regarding objects and events as objectively given phenomena, will we separate emotions from the world and oppose them to 'objective phenomena'. We make the same 'mistake' when discussing hallucinations, which are phenomenologically not any different from the seemingly objective objects and events with which we interact adaptively and about which we can communicate with each other. These are not new ideas at all; philosophical idealism has long understood these matters; but now we can relate them elegantly to the hippocampus, which is not only the generator of the world simulation but also the engine of our emotional feelings. But I don't think this explains why people are obnoxious or neurotic or mentally ill: here an understanding of how self-experience and our related sense of safety are regulated plays a critical role; this understanding is ultimately elegant again (you rightly hinted at the concern we all have with how we are seen), but to substantiate it we cannot rely on philosophy alone but have to consult the best of what psychoanalysis has to offer (self psychology in particular). The evolved mechanism that has brought about and underpins the experience of a self is the concern of my work presently and I hope it will all become clear in a book I'm writing.
yours, Ralf
Excellent! Thank you, Ralf, for explicating about emotions and the simulation; good stuff! And yes, I'd love to read the .pdf that you wrote about this.
What you wrote reminded me of the interview that Jesse Prinz gave me, talking about how we project our aesthetics and values on the world. How we tend to mistake things for being inherently beautiful or repulsive or whatever, rather than understand that we are representing them with that added value.
It's like Capgras syndrome, how the absence of the emotional marker in the simulation of mom means that I must radically re-explain reality, in order to explain how I feel. That is powerful stuff.
I've been thinking about the amygdala and insula, not just as emotional centers, but also as "meaningfulness" centers. They seem to do a good deal of the "painting" of the simulation, giving it context and helping to evoke previous similar memories.
I'm also curious, and wonder if you know about this: lateralization of function in the hippocampi. I've read occasional accounts which suggest that there is some task-specialization between the two. But I have to wonder: do they each simulate? Is it simultaneous? Are they simulating different versions of the same reality, say the left one for objects in the scene and the right one for meaningfulness or relationship? Interesting also that the two hippocampi have their own commissure, and do not rely on the corpus callosum.
I am very interested in the subject of the self, and am looking forward to hearing what you have to say about it. I've been thinking a lot about the fMRI studies that show the default network (and particularly the vmPFC) in conversation with the hippocampus, in daydreaming, projection,, theory of mind and other simulations. I think this suggests that the hippocampus is the "mind's eye" to the default network, the workspace within which "I" am able to manipulate representations. This, plus the fact that the vmPFC seems to store models of other people, makes it seem like a likely candidate for much of the sense of self.
In Buddhism, they invite the practitioner to look inside for the self; after unwrapping that concept for awhile, the students usually arrive at "the observer", the one who is perceiving consciousness. Which of course sounds a lot like Dennett's dreaded homunculus (except the observer does not have the ability to control the body). But I think it's a fair question: if the vmPFC is the manipulator of the hippocampus, could it also not be considered the observer of it? Isn't that what feedback is? This is one of my major questions about subjective experience: is it the simulation, being created within the hippocampus? Or is it the output of the hippocampus, being witnessed by another brain structure, like the vmPFC?
I'd love to hear your thoughts on all this. Thanks again, so much, for engaging in this conversation with me!
best,
matt faw
Dear Matt,
the vmPFC merely coordinates affective behaviour modes, I think, and implements them based on 'positional' information received from the hippocampus. The connection between the two is mostly unidirectional (some feedback via n. reunions). I don't think the vmPFC is involved the self other than through its role in anxiety. Have a look at that pdf, which discusses the vmPFC in some detail, and also shows how the insula and amygdala fit into the bigger picture. It also discusses the default mode network and its interaction with the hippocampus. As I said, it's not easy to read, and perhaps too long.
Regarding the self, before looking for its neural implementation, or for any 'mind's eye', we need to understand what the self is; this has to be the first step and this is the project I'm working on. I arrived at a fairly simple and evolutionarily sensible formulation having reviewed a great deal of psychoanalytic theory; what turns out to be central to our understanding of the self is the concept of narcissism, I mean normal or healthy narcissism which constitutes and important if not the most important dimension in the unconscious motivation of social behaviour in general; this can be shown beautifully in character structure, mental illness, group and social phenomena, child development etc.
Ralf
Dear Ralf,
My apologies for taking so long to get back to you. My sister had surgery last week (it went well), and I went to the east coast to support her.
I just got back and read your "situationally appropriate behavior" paper. It's very exciting, because it explains behavior and conditioning. I also sent the paper on to my dad (my science advisor on the documentary), along with your question about publishers. He and my mom are still taking care of my sister, so I don't think he's had any chance to get to it yet. But he's also working on a book, about the neural correlates of emotions, and I know he'll find your paper very interesting. Hopefully he'll also have some insight into publishers.
As a layman, I did find some parts of your paper hard to follow, mainly because most of my research, thus far, has been on the hippocampus and related MTL structures. So there were a lot of structures and concepts that were new to me. I wrote down notes for myself, and sent them off to my dad (copied below). If you see that I was way off on my understanding of the paper, I'd appreciate the correction.
I also did a rash of quick research on pathologies of the vmPFC, and found some interesting data that seems to support the idea of that structure as the driver of emotionally significant simulations, of both self and other. In the gambling task scenario, vmPFC patients have a hard time imagining their own future emotional response to losing or gaining money (even though the actual response is not later inhibited). In the Ultimatum game, vmPFC patients are mis-led by their immediate emotional response of fairness-violation to turn down relatively large percentages of offered money, perhaps because they are not able to create a prediction of how losing the money will make them feel later. ToM emotional tasks are inhibited (in damage to the right vmPFC), like being able to perceive irony or faux pas. And these patients have trouble seeing the moral violation in the person who intends ill, but does not succeed (like the person who intends to put poison in someone's coffee, but accidentally puts in sugar, instead), as if they are unable to take on the emotional perspective of the perpetrator. And even the emotional outbursts of frustration that seem to plague vmPFC patients may have to do less with emotional volatility (since they have overall flattened affect) and more to do with inability to predict how inappropriate their emotional response will be, how others will perceive them.
I was wondering how the vmPFC relates to emotional memory recall, and your paper answers that pretty well. And your paper is clear that it is at the heart of situational conditioning and regulating behavioral repertoire. That's a lot of function.
Thank you again for sending the paper, and for this continuing dialogue. I hope you are well!
best,
matt faw
Dear Matt
I'm sorry to hear your sister had to have an operation; i hope she is recovering well.
i think the vmPFC is relevant to decision making insofar as it confidantes and implements the anxiety response to simulated outcomes; anxiety-related bodily changes (somatic marker) feed back from the soma to the insula and on to the hippocampus; anxiety - which can be experienced as conscience (the feeling that one's action is liable to punishment, albeit from an abstract and internalized agency - the superego) - has the effect of inhibiting actions (drive-related actions, such as aggression) ('behavioural inhibition'). Simulation of an inappropriate and unacceptable action involves the vague experience of social criticism, which is what is experienced as anxiety, much like committing a punishable act causes anxiety.
so the neural correlates of emotion are complex (involving also the nucleus accumbens - another major output structure of the anterior hippocampus, as well as the lateral septum, and through the lateral septum and nucleus accumbens the hypothalamus importantly) but the experiential aspect of emotions (emotional feelings) seems to be subserved by the anterior hippocampus (which then links an emotional appreciation of the situation to the vmPFC and nucleus accumbens for an emotional behavioural and somatic response or to the prelimbic cortex for an instrumental/habitual behavioural response). Anthony Gray suggested that the anterior hippocampus adds an emotional dimension (which is what i think is experienced as emotional feeling) to visuospatial aspects of the situation (the location) ascertained by the posterior hippocampus.
so your dad writes a book about emotions? has he written something on that subject before?
kind regards
ralf
p.s. Below is the copy of my notes of your paper, that I sent my dad. He and I refer to the hippocampal formation as HF.
Hey pops, I doubt you've had the chance to read Behrendt's "appetitive behaviors" paper yet. I'm making my way through it now, and I wanted to collect some notes and thoughts as I do so: - One of the major themes, thus far, is in explaining behavioral conditioning in rats, via interaction between the hippocampus, vmPFC, and amygdala. Since behaviorism experiments tend to adjust one variable at a time, Behrendt I think is trying to explain how conditioning happens in the real world, in which the "situation" is the conditioned stimulus. The situation being a complex multimodal multidimensional stimulus, a combination of allocentric location map, place cell firings within that map, head direction or view direction cells, motor response, sounds, smells, vibrations and lighting, etc. Behrendt says the hippocampal output = the situation = the stimulus that is conditioned to. That conditioning happens in replay, after the salient event. After the rat has run the track to get its reward, the place cells that led it up to the reward now fire off backwards, to connect the memory of the reward to the steps that led up to it. This replay seems to be managed by the vmPFC, and while this new memory is still labile, the vmPFC brings in meaningfulness information from the basolateral amygdala, which gets encoded with the new memory for context. This maps "how did it make me feel" onto the memory encode, and strengthens the probability of that memory being recalled and being put into use later. Before running on a familiar track, the rat's place cells also pre-play the necessary behaviors to get to the reward, as mental rehearsal / prediction. Goal-oriented behavior is seen as depending on a loop between HF and mPFC, which keeps the expected outcome and its behavioral map in working memory. The medial PFC is explained, among other things, as the store house for mature associative representations. The index of memory eventually gets consolidated / copied to the mPFC, so it is no longer dependent on the HF for storage. Also, the mPFC receives output from the HF, and builds maps and indexes of various kinds, which then become short-hand models or assumptions about allocentric space, behavior sequences, meaningfulness of situations, and in humans, at least, maps of other people. More data that supports the view of HF as predictive agent. The rat's dorsal HF increases firing in anticipation of a reward. The closer the rat gets to the reward site, the more activity. Also, if new information arrives that fits within a pre-existing schema (i.e. if it matches expectations), then the HF activity is decreased, compared to when expectations are violated. The implication seems to be that the vmPFC can integrate this new semantic information into its mapping system, without as much need to re-simulate what just happened, with the new data included. It is when expectations are violated that the HF becomes more active, re-simulating its prediction to include the new data.
The orbitofrontal cortex may hold the mapping of reward (medial OFC) and punishment (lateral OFC) with objects. These two sections of the OFC seem to be mutually inhibitive. Sharp wave-ripple complexes are part of the HFs replay and consolidation process during times of rest, slow-wave sleep, and while consuming. They are associated with time-compressed but forward in sequence replay. The mPFC strong connection to motor and sensory areas may reflect its replay not only in the allocentric place map, but also replay of contextual stimulus and behavioral motor firing. Replay in the HF and mPFC is mirrored by replay in the ventral striatum, which Behrendt thinks is replaying the meaningfulness of the memory, its reward or punishment value. Motivation is provided by the nucleus accumbens core (reward) and shell (motivation toward reward). The prelimbic cortex (PLC) of the mPFC projects to the core, and the infralimbic cortex (ILC) to the shell. The core and PLC (which holds the behavioral maps) orient toward previously learned rewards, whereas the shell and ILC are necessary to orient toward open foraging without expectation of reward. PLC motivates precise behavior sequences, whereas ILC motivates more global behavior, like fight or flight. Stress increases ILC activation. PLC activation inhibits the ILC. Stress encourages the locus coeruleus to release noradrenaline into the PLC, effectively inhibiting it, and thereby removing the PLC's inhibition of the ILC. The ventral HF, when activated by stressors (via the locus coeruleus or basolateral amygdala), regulates the hypothalamic-pituitary-adrenal axis. It also increases, via a multisynapic pathway, activation of VTA dopamine output to the nucleus accumbens shell, increasing motivation to act. I get somewhat confused, when Behrendt is talking about dopaminergic pathways of motivation, but this much I think I follow: mPFC can activate the ventral tegmental area into delivering dopamine to the nucleus accumbens and into the mPFC, in order to keep motivation oriented toward the goal. Novelty signals or violations of predictions increases CA1 to VTA activation, increasing dopamine flow. And the central nucleus of the amygdala can also increase VTA activation. Dopamine increase in a rat's "preferred place" may mirror the increase in human social bonding and mating to "preferred people". The subgenual (subcallosal) anterior cingulate (area 25) is the primate version of the rodent's infralimbic cortex. It and the wider vmPFC are involved in initiating global fight or flight modes, as well as orienting in response to painful stimuli, including social discomfort. The subgenual anterior cingulate activates during anxiety and is chronically over-active in depressed patients. The anterior agranular insula receives motivationally salient information about interoceptive body states, including pain, thirst, hunger, cold, anger, fear etc. It provides bias and constraint to the vmPFC, in the picking of appropriate behavioral sequences. The insula effects the HF simulation via input through the lateral EC. In rats, instinctive behavior (like eating or drinking) is activated by connections from the ILC to the medial hypothalamic zone, and general appetitive arousal is invoked by ILC to lateral hypothalamus connections. The infralimbic cortex also projects to the autonomic and visceromotor centers in the hypothalamus and brainstem. In particular, it projects to the dorsolateral hypothalamic nucleus, a central part of the "visceromotor pattern generator network". The ILC also regulates the hypothalamus' "neuroendocrine motor zone". Motivational body states are part of the current hippocampal situation, and can motivate task focus. Planning is done in the default network, by invoking previous memories in the HF, and re-constructing them into a rehearsal. The plan, a newly minted behavior/context map, is followed by the task positive network, until violations of expectations force the switch back to the default mode, where the vmPFC uses the HF to re-simulate that part of the plan. The human dorsal anterior cingulate cortex helps provide attention toward ongoing task-relevant stimuli. That section (plus the wider dorsal mPFC) is also sensitive to violations of expectations. The rostral anterior cingulate, in conversation with the HF, learns about aversive stimulus to avoid, in the pursuit of the task, and then helps guide that avoidance behavior, along the route to the goal.
Dear Ralf,
Thank you for your kind wishes about my sister. She is indeed, recovering well.
Yeah, dad has been focusing more and more on the neural correlates of emotions, over the last several years, and has been presenting talks on the insula, etc. at various conferences. When I sent him the notes I generated, while reading your paper, his response was: "Wow! I love your description of Behrendt's paper. I must now read it. Every bit of it deals with my book. I am dealing with each of those areas you mentioned. Behrendt puts it together in a way that I must incorporate." He's recently been really focused on my sister, of course, but he's a voracious researcher, and I'm sure he'll devour your paper hungrily.
Ralf, I have a favor to ask of you, beyond being interviewed for the documentary. As I'm sure you can tell, I've been thinking about the hippocampus' role in consciousness for some time now. I had reached an impasse in the documentary, where science was not connecting the dots, and I knew that simulation had something to do with it. Then, in a conversation with my dad last February, I mentioned how similar I thought that recall and imagination were, and dad told me about the recent work tying the hippocampus to these various simulation tasks, and the light bulb went off. By the end of that day, I was convinced that subjective experience was a simulation, generated in the hippocampus, for the sake of memory.
When I started looking for researchers connecting consciousness and the hippocampus, I did not find you immediately, and so it seemed like no one was yet saying what seemed to me to be a powerful explanatory model, the only model I've heard that really made sense to me. I thought I saw an elegance and clarity in the hypothesis, which explained all these major mysteries of subjectivity. But, I had no one to interview about it, so instead I interviewed other specialists on the hippocampus, like Demis Hassabis and Itzhak Fried, and worked on a paper to float the idea to the scientific world, see if anyone would respond.
Now, of course, that I've found you, I am grateful to have a chance to finally interview someone who has already approached the same hypothesis from an neuroanatomical bent. And I am very much looking forward to the chance to interview you.
However, something is still missing. I cannot release a documentary claiming what science is saying about consciousness, unless the broader community has first tested that theory. So I still want to submit my paper to a journal, and present a poster at the Tucson TSC conference, etc., start a P.R. blitz with this theme, in order to try to encourage others to test this theory. That way, hopefully, by the time the film comes out, this theory really will be reflective of what science says. (and if it's not, and I'm wrong, then I want science to show that, so I can change my film).
I was trying to finalize our paper (dad wrote the neuroanatomy section), and was looking for final citations, when I found your 2013 paper on consciousness and the hippocampus. Dad and I both feel that our paper is about ready to submit, but I sure would feel better, having an educated 3rd party read over it first. I don't know of anyone else on the planet who even knows the theory, and therefore no one else is better suited to give constructive feedback about it. I'm sure you are a very busy person, but if you think you might have time to look over our latest version of the paper (which of course, you are now heavily cited in), I would be extremely grateful.
Respectfully yours,
Matt Faw
Dear Matt
i would love to have a look at the paper. I am really glad too to know that there is somebody who appreciates the beauty and elegance, as you put it, of the simple idea that subjective experience is but episodic memory formation in action. I am also delighted by the fact that your father likes my paper too (i take it you meant the frontiers one?).
so yes send me that paper; i'll read it as soon as i find some time
Best wishes to you and your family
Ralf
Thank you so much, Ralf! I really appreciate it.
You'll see that this is version 38. We actually submitted a different version of the paper earlier, last August, but were rejected. Not because of the theory, but because I had never written a paper before, and my prose was reviewed as being too "unserious".
I completely re-wrote my sections of the paper for this new version, and I think it's now pretty clear, and well supported. I hope you agree. It helps a lot that I now have your paper to cite, for some of the more speculative aspects of the theory. The first two sections, which are both philosophical arguments, are mine, and the last section, which is an argument from neuroanatomy, is mostly written by my dad. I don't think dad has yet read your paper on consciousness, unfortunately, so this draft does not reflect your influence there. Your paper is much more comprehensive and thoroughly researched, so I'm happy to have your feedback there, and throughout.
The file is in .pdf format. Please let me know if you have any problems accessing it. Feel free to highlight, cross-out, add, etc.
Thank you again, so much, for being willing to look at our paper. I look forward to hearing your response.
sincerely,
matt faw
Dear Matt
the paper is very long; you could tidy up part 1 and condense part 2 to whatever is most relevant for the idea that the hippocampus is the site of simulation of the world; some of the material in part 2 is interesting only for those who still believe that what we see is the world as it is (as opposed to it being a memory or a product of hippocampal simulation), which suggests to me that you could reorganize the whole manuscript; i would dispel that myth of realism first, combining everything from parts 1 and 2 that helps us to understand the subjective, non-reality (simulated) nature of consciousness; second i would proceed to argue that consciousness (externalized and imaginary) equals episodic memory formation and recall (and third briefly summarize whatever suggests that the hippocampus is critically involved in episodic memory formation and recall); fourth i would gather up from your material evidence specifically for involvement of the hippocampus in consciousness including imagery (not evidence implicating the hippocampus in episodic memory processes); i made some changes to your file, but as i said, i would tackle the whole matter in those four steps so that you can get greater clarity for yourself and for your readers; the material from your part 3 as it stands i would only include where it is essential to understanding why certain evidence can be taken as implicating the hippocampus in consciousness.
i also attach a paper that shows that our way of thinking about consciousness has a long history.
Looking forward to hear from you
kind regards
ralf
Dear Ralf,
Thank you very much for reading the paper, and for the feedback. I really appreciate you taking the time.
Now I have to wrestle with how best to implement and integrate your notes. I'm also forwarding your comments to dad, see what inspiration he can get from them.
Thanks also for sharing your previous work on idealism. The epistemological implications of simulation has been at the heart of my own 'spiritual' path for years, learning to surrender certainty and stories, in order to experience beyond my habits. Trying to surrender my sense of self for a new model of my brain as a community, and learning to trust the brain parts that I can't directly observe. That's why, when I first heard that there was an experience simulator in the brain (in that conversation with my dad last year), that it was a short leap of logic to the hippocampus as home of consciousness, and from there, seeing subjective experience (and self) as memory.
When I started conducting interviews, I expected everyone to talk about experience as a construction, but I got surprisingly little of that, mostly from the specialist on psychedelics. I think Dennett's Cartesian Theater argument is so compelling that it has put many off the scent, which is why I had to address that argument. Thomas Metzinger, who I quoted at the top of the paper, is one of the few I've seen who is championing the idea of simulation of experience and self. Others hint at it, but I think the illusion of consciousness as command and control unit is so powerful, that it is hard to go deep down that rabbit hole. That's why "driving mind" and Libet's experiments are at the top of my list of evidence, because both specifically illustrate that the sense of an agentive 'I' is a feature of memory, and is not needed for choice.
A thought about the self: what I think of as a personality, at least from the 3rd person perspective, is a constellation of habits, including habits of simulation. From your "situational behavior" paper, it's interesting that the vmPFC stores and elicits behavioral maps, which I interpret as habit. Of course, there is habit throughout the brain, Hebbian, concept cells, conditioning, semantics, etc. But behavior maps, in particular, seem to be the defining features of a personality.
I'm curious if you know how the default network and the hippocampus relate to Michael Gazzaniga's idea of a left-hemisphere narrator module. That seems to me to be an important part of the story (not for this paper, but for the documentary), how language can serve as a low-bandwidth mnemonic, simplifying memories into stories. That simplification, and the need to tell a story that fits within the context of one's self-model, is I think, the source of a good deal of error. I had included his theory in previous versions of the paper, but left it out this time, in order to be leaner and more concise. I'm hoping to interview him, as well, for the doc.
Thanks again for your time and energy, and for this continuing conversation!
Much respect,
matt faw
Dear Matt
yes what you say about the left hemisphere default network seems plausible; the left hemisphere default network is concerned with exploring events related to each other in time, whereas the right network seems to do the same for space. our thinking about time, and hence also our narrative thinking about ourselves, is a derivative of spatial relational thinking, the animal's location in space and then the relationship between objects in space and between animal's locations on a map being the original functions of the hippocampus (the first one actually being the determination of the animal's location by scent)
i only thought it might be better for didactic reasons to first discuss the ideas that the self is not an agent and that the world is a simulation and then to implicate the hippocampus;.... actually i think the whole argument can be made without the self; but of course the self is an interesting subject in itself and you can easily deduce that the self is an aspect of the simulation and hence supported by hippocampal function; perhaps you could tackle consciousness and the relationship between hippocampus and consciousness in the first part of the paper and deal with the self, philosophically and neurologically, in the second part of the paper; that would be an alternative way of organizing the material that you have meticulously assembled but which i find could be organized more logically; i think my slight difficulty with your excellent paper only derives from my insistence that consciousness has got little to do with any self and that the self is not a necessary component of consciousness, while of course the self, insofar as it does enter the scene, is predicated on consciousness.
Ralf
Hi Ralf,
Thanks for your e-mail, and for the greater context for your previous comments. I took the weekend away from the paper, to give it some air, so I'll be taking a deeper look today. I will definitely keep your suggestions in mind, as I make my revisions.
Our previous (rejected) paper attempted to detail a much more thorough theory, with a philosophical explanation from the neuron up, and going much deeper into the concept of self. Unfortunately, that approach buried the headlines, and lost our reviewers.
So, my attempt with this version has been to feature all the major headlines right off the bat, make sure that the reader gets a quick primer, before getting any deeper into the argument. And so far, it feels like the headlines have to be: subjective experience is a simulation, a brand new memory created predictively and edited retrospectively in the hippocampus from stripped-down reports from around the brain (and that salience for memory is based on deviation from expectations), that it represents reality to the rest of the brain (and can make significant errors), that the sense of self is only an element of that memory, and that therefore the terms "conscious" and "automatic" have to be rethought. These feel, to me, like the minimum details necessary to explain a radically counter-intuitive way of looking at consciousness; without any of them, the argument feels incomplete. And of course, these details have to be supported with some evidence, like the imaging studies on the hippocampus as experience generator.
The second section, as argument from evidence, is really aimed at the people like me, who may not know all the anatomy, but who know all the standard problems of subjectivity. I'm hoping that by saying "if you look at it from over here, it all lines up" that the reader will see that there is real explanatory power in this equation. I also think that this section supplies the testable hypotheses of the paper.
The third section, of course, is for people like you, who have a strong sense of how the brain works. The attempt here is just to say that overall argument is plausible, given what we know. Of course, it cannot be nearly as comprehensive as your paper on the same subject. But please let me know if you disagree with any of the science there, or elsewhere in the paper.
You made some cross-outs in the paper; I'm wondering if those were because you felt the science would not support those statements, and/or they were too speculative, or if it's just that you thought they were not necessary.
Thank you again so much for your feedback and your time!
best,
matt faw
Dear Matt
i thought those points (the ones i crossed out) were not necessary; you are right though in feeling that you need to take a broad approach to the subject but i would only include facts that are highly relevant to the thesis: 1. why consciousness or the self are not in control they way they were thought to be (and why conscious/unconscious processing has to be rethought); 2. that consciousness is a simulation of the world; 3. that consciousness coincides with episodic memory formation and recall; and only 4. why the hippocampus needs to be implicated.
that way the argument would be arranged more logically, i feel; and that way you can include in part 4 only what is really relevant and supports the argument reasonably tightly; so i would not write at the same time a survey of hippocampal function
but you are absolutely right; a paper like that needs to be written; for it to have an impact it needs to be organized very logically, and i would structure it the way i suggested; you've got all the material already, just try and fit it in this raster and see if it can be substantially shortened that way
please let me know how you get on
sorry about late reply but have been very busy this week
speak to you soon
ralf