Beyond brain regions: Network perspective of cognition–emotion interactions

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).

Emotion and automaticity

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.

Low road vs. high road: Many roads lead to the amygdala

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.

Low road vs. multiple roads

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.

Amygdala and attention

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.

The amygdala: From “What is it?” to “What’s to be done” functions

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.