Thursday, December 26, 2013

brain01 pessoa brain Pathway Emotion & Cognition and the Brain, by Luiz Pessoa

Of snakes, the pulvinar, and fear

Posted on November 25, 2013 by cognitionemotion
A new paper in PNAS suggests that “Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes” (from the title). I’m happy that more research is being done on the functions of the pulvinar, a structure that is fascinating. There are many interesting findings in the paper, and it’s certainly worth reading.
snake
The problem, as usual, is not with the results but with their interpretation.Establishing selectivity to visual stimuli is challenging at best (cf. all the disputes re. faces in ventral visual cortex). Some puzzling (and to me telling) aspects of the data that the authors barely discuss are:
  • Good responses were observed to high spatial frequency stimuli (!), not just low pass images. In fact, the effect of low vs. high pass had a small effect size (given a p value that was only < .1)
  • Latency to snake pictures was fast (around 55 ms on average) but how much faster than other stimuli it was not clear (but maybe I missed this).
  • The authors suggest that they recorded from the medial pulvinar (the “associational” sector). Talking to colleagues who are familiar with the intricacies of pulvinar anatomy in several species, the  figure shown by the authors does not make this point convincingly. The authors really need to demonstrate that this is not visual pulvinar (that is, from what is shown it is not clear that they were in the medial pulvinar as described in the literature).
These are issues that can be resolved with further research. My main concern is the evolutionary conclusion of the paper.  As phrased by the authors: “Our data provide unique neuronal evidence supporting the hypothesis that snakes provided a novel selective pressure that contributed to the evolution of the primate order by way of visual modification”. This is unfortunate; I’m not a comparative neuroscientist, but without studying multiple extant species, a claim like this is clearly over-reaching.
Reference: Van Le, Q., Isbell, L. A., Matsumoto, J., Nguyen, M., Hori, E., Maior, R. S., … & Nishijo, H. (2013). Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes. Proceedings of the National Academy of Sciences, 110(47), 19000-19005.
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Brain evolution: amygdala bigger than PFC??

Posted on November 16, 2013 by cognitionemotion
This year I attended the pre-SFN meeting on Evolutionary Neuroscience by the J.B. Johnston Club. I enjoyed the meeting a lot (though was somewhat baffled by their obsession with isometric lines with slope 1…) and ended up bumping into a couple of comparative papers on the amygdala (that I should have known about).
Although fairly crude, one can gain insight into brain evolution by measuring volume or counting cells across brain regions and species. This has led to much debate, for instance, regarding the PFC and its possible “enlarged status” in humans. If you do that for different amygdala nuclei, you find that “the human amygdala is evolutionarily reorganized in relation to great ape amygdala”.
This quote is also quite revealing: “Neuron numbers in the human lateral nucleus were nearly 60% greater than predicted by allometric trends, a degree of magnitude rarely seen in comparative analyses of human brain evolution (Sherwood et al., 2012). For example, the volume of the human neocortex is 24% larger than expected for a primate of our brain size (Rilling and Insel, 1999), whereas the human frontal lobe, long assumed to be enlarged, is approximately the size expected for an ape of human brain size (Semendeferi et al., 2002; Semendeferi and Damasio, 2000).”
So much for such a highly conserved structure… Interesting also that the authors discuss “evolutionary specializations” of the amygdala in terms of the social brain, not “fear processing” (as for instance described in this previous post).
Reference: Barger, N., Stefanacci, L., Schumann, C. M., Sherwood, C. C., Annese, J., Allman, J. M., … & Semendeferi, K. (2012). Neuronal populations in the basolateral nuclei of the amygdala are differentially increased in humans compared with apes: a stereological study. Journal of Comparative Neurology, 520(13), 3035-3054.
The other reference is also interesting: Barger, N., Stefanacci, L., & Semendeferi, K. (2007). A comparative volumetric analysis of the amygdaloid complex and basolateral division in the human and ape brain. American journal of physical anthropology, 134(3), 392-403.
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The Cognitive-Emotional Brain

Posted on October 7, 2013 by cognitionemotion
It’s out! Finally, The Cognitive-Emotional Brain: From Interactions to Integration, from MIT Press, is out. I remember a few years ago when talking to Olaf Sporns about writing a book and him encouraging me… (he was just finishing his first one on networks for MIT Press as well). It’s a long journey, but I found it really rewarding and in a way refreshingly unlike the cycle of paper-reject/grant-reject that many of us are used to… Who knows, maybe it’s time to start a new one! I hope that some of you will enjoy it…

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Amygdala evolution and cortical-subcortical integration

Posted on September 25, 2013 by cognitionemotion
I finally had a chance to take a more careful look at this paper by
Chareyron, L. J., Banta Lavenex, P., Amaral, D. G., & Lavenex, P. (2011). Stereological analysis of the rat and monkey amygdala. Journal of Comparative Neurology, 519(16), 3218-3239.
I think the figure here summarizes a major point of the paper. Although the scale bar is not the same for the 3 species, it is evident that the lateral amygdala (red) is disproportionately represented in the human case. To the contrary, the central nucleus is less represented. The basolateral amygdala has extensive connectivity with cortex, whereas the central nucleus is more “autonomic”. One can speculate that the increase in relative size of the basolateral amygdala paralleled increases in cortical representations. In fact, this could be an example of the proposal by Harvey and Barton that brain structures with major anatomical and functional links evolve together (independently of evolutionary changes in other unrelated structures).
I completely agree with the paper’s suggestion that their results are consistent with the “hypothesis of a higher convergence and integration of information in the primate amygdala.”
On the other hand, I don’t agree with their conclusion that “although the fundamental function of the amygdala, to regulate fear and emotional learning, is conserved across species, amygdala function might be under greater influence of cortical activity in primates, and therefore integrate additional contextual information that influences the regulation of more complex behaviors such as social interactions.” I believe the statement is still too attached to the traditional view of the amygdala as a simple “alarm system”. Such view neglects the amygdala’s sophisticated involvement in a host of perceptual and cognitive functions (see this paper) and underestimates the potential for altered connectivity to change the functional repertoire of the amygdala.
Left: Rat (top), Macaque (middle), and Human (bottom) amygdala. Right: schematic illustration of cortical-subcortical connectivity.
Left: Rat (top), Macaque (middle), and Human (bottom) amygdala. Right: schematic illustration of cortical-subcortical connectivity with the amygdala. From Chareyron et al. (2011).
 
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Amygdala modulation of visual cortex

Posted on September 18, 2013 by cognitionemotion
Further evidence that the amygdala modulates visual cortex. Unfortunately, it is not unit recording, it is actually an optical imaging study. The study was performed in the cat under anesthesia, not ideal either.
Y. Chen, H. Li, Z. Jin, T. Shou, H. Yu (2013). Feedback of the amygdala globally modulates visual response of primary visual cortex in the cat. Neuroimage, in press.
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From Brain Networks to Cognitive Function

Posted on May 27, 2013 by cognitionemotion
Olaf Sporns was asked to organize a symposium on networks for the annual meeting of the Association for Psychological Science 2013 and invited four of us to present our work: Paul Laurienti, Barry Horwitz, Randy McInstosh, and I. Lots of parallel sessions, so the room was somewhat small, but I believe it went well.
I described the work that I’ve done with Michael Anderson and more recently with Lucina Uddin (together with Josh Kinnison from my lab). Here are the slides:APS 2013
One part that I like is the possibility of characterizing the multidimensional functional fingerprint of a brain network — not a region.
network fingerprint
Fingerprint of the “attention network”.

Down with “centers” (= brain areas)

Posted on May 16, 2013 by cognitionemotion
Great Opinion paper by Marlene Berhmann and David Plaut on “face” and “word” processing. The upshot is that we should understand these as distributes circuits, not in terms of circumscribed centers as they state in the title.
Behrmann, M., & Plaut, D. C. (2013). Distributed circuits, not circumscribed centers, mediate visual recognition. Trends in cognitive sciences, 17(5), 210-219.
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Carl G. Lange: First proponent of the “low” vs.”high” road?

Posted on March 20, 2013 by cognitionemotion
I finally got to reading Lange’s The Emotions: A Psychophysiological Study from 1885 (English 1922 translation of the German version) and found the most amazing thing: a dual-pathway, “low” and “high” road model of emotional processing:
From Lange (1885)
From Lange (1885). The “low road” goes from the eye to CO’ to CV — all subcortically. The “high road” goes up via cortex before coming down to CV.
The pathway from the eye to CO’ leads to CV rather directly. CV is a motor stage somewhere unspecified but in the brainstem. This applies to “simple” cases. But when a “mental process” is involved, cortical stages of vision and taste must be engaged, namely CO” and CG”. Now, the “impulses” get to CV from cortex!
I didn’t know about this passage, which I found rather stunning!
Here’s what Lange says himself: “… those emotions which are due to a simple sense impression, a loud noise, a beautiful color combination, etc., the path to the vasomotor center must be quite direct, and the cerebral mechanism but slightly complicated… The matter becomes somewhat more complicated when those affections are involved which are produced not by a simple impression upon some sense-organ, but by some ‘mental process,’ some memory or association of ideas, even if the latter be due to
sense-impression.”
Do you know of earlier formulations of this type of dual-route model? If so, let me know!
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Understanding the function of brain regions and brain networks

Posted on March 1, 2013 by cognitionemotion
Michael Anderson, Josh Kinnison and I have just published a paper in Neuroimage describing a framework for capturing a brain region’s functional fingerprint, in addition to the fingerprint an entire network of brain regions. These are computed based on studies published in the BrainMap database and provide an estimate of the functional repertoire of a given brain region/network. For example, here’s the fingerprint of the dorsal ACC:
Functional fingerprint of the dorsal anterior cingulate cortex. The red and blue lines represent the uncertainty range of our estimate).
Functional fingerprint of the dorsal anterior cingulate cortex. The red and blue lines represent the uncertainty range of our estimate.
The framework allows the quantification of functional diversity (captured via Shannon’s entropy) in a voxelwise manner (by moving a 10-mm radius “spotlight” around). We found that most brain regions had diverse functional profiles, though diversity varied considerably across the brain (below, the zones in red are the most diverse):
Voxelwise functional diversity.
Voxelwise functional diversity.
The functional profiles of brain networks can also be characterized, such as the one of the “ventral attention network”:
Functional fingerprint of the ventral attention network.
Functional fingerprint of the ventral attention network.
Our study thus allowed us to characterize the contributions of individual brain regions and networks of brain regions without using singular task- or role-bound functional attributions.
Here’s the reference in case you have problems with the PDF link:
Anderson, M. L., Kinnison, J., & Pessoa, L. (2013). Describing functional diversity of brain regions and brain networks. NeuroImage, 73, 50–58.
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Beyond brain regions: Network perspective of cognition–emotion interactions

Posted on August 16, 2012 by cognitionemotion
Stephan Hamann has just written an interesting piece on mapping emotion to the brain (here). His conclusion is that
“Although neuroimaging studies have identified consistent neural correlates associated with basic emotions and other emotion models, they have ruled out simple one-to-one mappings between emotions and brain regions, pointing to the need for more complex, network-based representations of emotion.”
I also think that “networks” is the right approach, and have written a short commentary that makes the following points (for refs, please see the commentary):
This comes from a recent paper of ours (Kinnison et al., 2012).
1) Given the extensive interactions among brain regions, the emphasis shifts from attempting to understand the brain one region at a time, to understanding how coalitions of regions support the mind-brain. Insofar as brain regions are not the unit of interest, they should not be viewed as “cognitive” or “emotional.” Traditionally, however, regions whose function involves homeostatic processes and/or bodily representations have been frequently viewed as “emotional,” whereas regions whose function is less aligned with such processes have been viewed as “cognitive.”
2) The architectural features of the brain are such that they provide massive opportunity for cognitive-emotional interactions (Modha & Singh 2010). These interactions are suggested to involve all brain territories. For example, extensive communication between the amygdala and visual cortex exists, and efferent amygdala projections reach nearly all levels of the visual cortex (Amaral et al. 2003). Thus, visual processing takes place within a context that is defined by signals occurring in the amygdala (as well as the orbitofrontal cortex, pulvinar, and other regions), including those linked to affective significance (Pessoa & Adolphs 2010). Therefore, vision is never pure vision, but is affective vision – even at the level of primary visual cortex (Damaraju et al. 2009; Padmala & Pessoa 2008). Cognitive-emotional interactions also abound in the prefrontal cortex, which is thought to be involved in abstract computations that are farthest from the sensory periphery. More generally, given inter-region interactivity, and the fact that networks intermingle signals of diverse origin, although a characterization of brain function in terms of networks is needed, the networks themselves are best conceptualized as neither “cognitive” nor “emotional.”
3) Regions that are important for affective processing appear to be exceedingly well connected (e.g., Petrovich et al. 2001; Swanson 2000). This suggests that these regions have important “quasi-global” roles and that this is an important feature of this class of region. However, regions traditionally described as “emotional” are not the only ones that are highly connected. Highly connected regions are encountered throughout the brain, including in the occipital, temporal, parietal, and frontal lobes, in addition to the insula, cingulate, thalamus, and regions at the base of the brain (Modha & Singh 2010).
4) Emphasizing only interactions between brain regions that are supported by direct, robust structural connections is misleading. For one, the strength of functional connectivity is equally important, and at times will deviate from the strength of the structural connection (Honey et al. 2007). Architectural features guarantee the rapid integration of information even when robust structural connections are not present, and support functional interactions that are strongly context dependent. This is illustrated, for example, by the “one-step” property of amygdala–prefrontal connectivity – amygdala signals reach nearly all prefrontal regions within a single connectivity step (see Averbeck & Seo 2008).
5) Taken together, these considerations suggest that the mind-brain is not decomposable in terms of emotion and cognition. In other words, the neural basis of emotion and cognition should be viewed as governed less by properties that are intrinsic to specific sites and more by interactions among multiple brain regions. In this sense, emotion and cognition are functionally integrated systems, namely, they more or less continuously impact each other’s operations (Bechtel & Richardson 2010). As suggested by Bechtel and Richardson, “The problem is then not one of isolating the localized mechanisms, but of exhibiting the organization and the constituent functions. . . [A]n explanation in terms of organization supplants direct localization” (p. 151).
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Emotion and automaticity

Posted on February 25, 2011 by cognitionemotion
The idea of automaticity — a notion that is often invoked in the context of affective processing — is a pretty tricky one. The issue is, of course, not limited to affective processing and is encountered in several cognitive domains (for example, word processing). Reading some of cognitive literature it feels that many (all?) of the processes that at some point were deemed automatic were shown to be capacity-limited once the system was pushed hard enough. It is in this context that I particularly like the quote by Moors and De Houwer (2006, p. 321):
“Every process is uncontrolled, efficient, unconscious, and fast, to some degree.”
In other words, an all-or-none view of automaticity is untenable, and a continuous approach is needed (as eloquently outlined by Moors and De Houwer). We thus need frameworks for understanding the continuous nature of cognitive/affective processing, for instance, as suggested originally by Norman and Bobrow (1975) and again by Nakayama and Joseph (1998).
I have briefly outlined related ideas in the context of affective processing in a recent talk at a meeting organized by Gilles Pourtois, Ernst Koster, and colleagues at the University of Ghent, Belgium.
 
Different processing pathways have different capacity limitations (inverse circle size).
References:
Moors A, De Houwer J (2006) Automaticity: a theoretical and conceptual analysis. Psychol Bull 132:297-326.
Nakayama K, Joseph JS (1998) Attention, pattern recognition, and pop-out in visual search. In: The Attentive Brain (Parasuraman R, ed), pp 279-298. Cambridge: MIT Press.
Norman DA, Bobrow DG (1975) On data-limited and resource-limited processes. Cognit Psychol 7:44-64.
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Low road vs. high road: Many roads lead to the amygdala

Posted on November 9, 2010 by cognitionemotion
As outlined in the previous post, Ralph Adolphs and I have written a critique of the idea that a subcortical pathway conveys affective information to the amygdala in a rapid, automatic fashion. Our argument can be summarized as follows (details are provided in the paper):
  1. Affective information is not processed faster than other types of visual information;
  2. The processing of affective visual stimuli involves both coarse and fine (i.e., low and high spatial frequency) information;
  3. Recent studies suggest that the amygdala is not essential for rapid, non-conscious detection of affective information;
  4. A related point discussed elsewhere is that the processing of affective stimuli does not take place in a manner that is as independent of attention and awareness as frequently advanced (for additional discussion, see paper);
  5. Evidence for an uninterrupted anatomical pathway in primates linking the retina to the superior colliculus to the pulvinar to the amygdala is lacking;
  6. A related point is that the medial pulvinar (the part that is anatomically connected to the amygdala) is a highly integrative thalamic region that is bi-directionally connected with many cortical regions, including frontal, cingulate, insular, and parietal cortices. In other words, the medial pulvinar is not a passive relay of visual information, but likely integrates multiple sources of information in important ways.
  7. More broadly, I have argued that emotion and cognition are not separated in the brain (see paper), and are better conceptualized as co-determining each other.
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Low road vs. multiple roads

Posted on October 29, 2010 by cognitionemotion
The processing of affective information has many attributes that make it special, such as speed, and relative independence from attention and awareness. A key question, therefore, both from basic and applied perspectives is how this happens. An extraordinarily popular account is that a so-called low road from the retina via the superior colliculus and pulvinar conveys information to the amygdala. The general idea is that, because the pathway is entirely subcortical, processing would then be automatic.
This proposal has captured the attention of the research community and has fostered several lines of investigation — what is the role of attention, of awareness, how fast are certain effects, what type of visual information is conveyed (low vs. high spatial frequency), etc. Although these questions are interesting, the subcortical pathway idea is, in my view, largely based on an idea, rather than solidly grounded on empirical data.
So for a while now, Ralph Adolphs and I have been discussing what are serious problems with the notion of automatic subcortical processing of affective information. We have now written up some of these ideas in this Opinion piece in Nature Reviews Neuroscience. We also propose a new scheme, called the multiple-waves model that is intended to be an alternative to the “standard view”. It looks like part (B) of this figure, in contrast to the more traditional view shown in (A).

The proposal also incorporates the fact that the pulvinar is a highly integrative thalamic region, with extensive interconnectivity with much of cortex, as shown below.
The pulvinar works in a way that integrates cortical-subcortical processing.
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Amygdala and attention

Posted on July 1, 2010 by cognitionemotion
An extremely interesting aspect of amygdala function is that mild electrical stimulation of this structure produces an “orienting response”. As described originally by Kaada and colleagues, “the animal usually raises its head and looks in an inquisitive manner”. The original photos by Kaada are quite revealing, as shown here in this drawing.
Attention response
ATTENTION RESPONSE. Stimulation of the amygdala with mild electrical currents elicits an “attention response”. (A) Before stimulation. (B, C) During stimulation. Adapted from Ursin and Kaada (1960). Illustration by Gatis Cirulis.
I suggest that this behavior is a manifestation of affective attention processes carried out by the amygdala and related structures, including the basal forebrain and hypothalamus (paper). Whereas some of these mechanisms mobilize neural resources, others are suggested to engage bodily resources, too.
Affective attention.
AFFECTIVE ATTENTION depends on the amygdala (A; blue ellipse) and other structures. Diffuse projections from the basal forebrain are shown in yellow; efferent projections from amygdala nuclei are shown in green; the central nucleus of the amygdala also originates descending projections (black arrow) via the hypothalamus and other brainstem nuclei.
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The amygdala: From “What is it?” to “What’s to be done” functions

Posted on June 25, 2010 by cognitionemotion
In this Blog I will discuss ongoing issues related to cognitive-emotional interactions in terms of brain and behavior. Mostly, I’ll discuss some of my ongoing research and related ideas and, occasionally, I’ll write an entry related to other published papers of interest.
In this first post, I’ll comment on a recent review that I wrote trying to summarize some of the functions of the amygdala (here’s the link:  paper).
So, what is the function of the amygdala? Beyond the “fear theme” that has dominated research in the past several decades, two papers that were quite influential in proposing a broader role for the amygdala were the one by Paul Whalen in 1998 and the one by Sander and colleagues (2003). In my review, I suggest that it might be fruitful to go beyond what both of these papers suggested and to consider the roles of the amygdala more broadly in terms of attention, and the representation of value and decision making. Naturally, all of these ideas have been described in the past, but I give my angle on these and other issues in the review. I picked up on a them discussed by Pribram and McGuiness (1975) on conceptualizing functions in terms of “What is it?” and “What’s to be done?” roles that I believe are useful.
In the context of thinking of more general functions of the amygdala, a recent quote that I particularly like, which I recently came across, is one from Amaral and Price (1984), in which they suggest the following:
“As our knowledge of the connections of the amygdala has expanded, it has become apparent that the earlier view that it is primarily involved in the control of visceral and autonomic function is incomplete… These widespread interconnections with diverse parts of the brain simply do not fit with a narrow functional role for the amygdaloid complex. They support, rather, the behavioral and clinical observations which suggest that the amygdaloid complex should be included among the structures which are responsible for the elaboration of higher cognitive functions” (pp. 492-493).
Refs:
Amaral, D.G. & Price, J.L. Amygdalo-cortical projections in the monkey (Macaca fascicularis). The Journal of comparative neurology 230, 465-496 (1984).
Pribram KH, McGuinness D (1975) Arousal, activation, and effort in the control of attention. Psychol Rev 82:116-149.
Sander D, Grafman J, Zalla T (2003) The human amygdala: an evolved system for relevance detection. Rev Neurosci 14:303-316.
Whalen PJ (1998) Fear, vigilance, and ambiguity: Initial neuroimaging studies of the human amygdala. Current Directions in Psychological Science 7:177-188.
Filed under: Amygdala | Tagged: , , , | 1 Comment »


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