Brain evolution: amygdala bigger than PFC??

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.

Amygdala evolution and cortical-subcortical integration

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).

 

Amygdala modulation of visual cortex

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.

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.