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.
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