Savoir Faire or Savant?

Is amygdala volume correlated with social network size or with special talents in autism spectrum disorders? Or both??

The amygdala is a subcortical structure located within the medial temporal lobes. It consists of a number of different nuclei, or collections of neurons delineated by commonalities in morphology and connectivity. The amygdala is best known for major roles in fear conditioning (Paré et al., 2004) and responding to emotional stimuli more generally (Phelps & LeDoux, 2005), but its functions extend beyond that.

A presentation at the recent Society for Neuroscience meeting in New Orleans reported on MRI data obtained from Dr. Temple Grandin, the famous and talented Professor of Animal Science at Colorado State (Cooperrider et al., 2012):

Dr. Temple Grandin: A neuropsychological and multimodal neuroimaging case study of a savant with autism

. . .

Results: Dr. Grandin’s left lateral ventricle showed much more leftward volumetric asymmetry than controls. Her left cerebral white matter volume and bilateral entorhinal cortex thickness were much greater compared to controls. Her fusiform gyrus thickness was much less than the control mean. She had greater left lateral ventricle, intracranial, left cingulate, bilateral amygdala, and bilateral entorhinal cortex volumes. White matter microstructural differences were found for Dr. Grandin in multiple brain regions, including those known to relate to language function and facial information processing. ... The neuropsychological assessment indicated superior visuospatial and nonverbal reasoning abilities...

Virginia Hughes wrote a splendid summary of the study, which is not yet published in a peer-reviewed journal.

An earlier experiment was conducted with another very talented autistic savant (Corrigan et al., 2012):

The subject of this study is a 63-year-old, right-handed male with savant syndrome and a long-standing diagnosis of ASD.¹ Institutionalized as a child, he has lived semi-independently as an adult, working for more than 30 years in dishwashing jobs. This individual is gifted with several special skills. One area of considerable talent is in music. He has perfect pitch and plays several musical instruments, of which his favorite is the accordion. He has substantial abilities with languages and can engage in basic conversations in twelve different languages. He also has remarkable abilities with sound imitation. His most exceptional ability, however, is in the area of art. ... He has become a highly regarded and accomplished graphic artist, whose works have been recognized through numerous exhibitions nationally as well as publication in a book. His medium is paper with pencil, marker, and crayon. His interest is in drawing collections, usually quite large, of items such as tools, birds, instruments, trains, flowers, and shoes, among many others. He takes a special interest in categorizing the physical world.

The volumes of his amygdala and caudate were both larger than values in the normative literature, and a strong right-sided asymmetry was seen for both structures (Corrigan et al., 2012). Hippocampal volumes did not differ from control values.

Although these two single-case studies were of exceptional people who may not be characteristic of the general ASD population, it was notable that both individuals had larger amygdalae than controls. Is this a surprising finding, in light of recent results on the correlations between amygdala volume and social network size in control participants? Surely the average neurotypical college student has a larger Social Network Index of offline contacts (Bickart et al, 2011) and more Facebook friends (Kanai et al., 2012) than the average person with ASD?

Grandin says, “the part of other people that has emotional relationships is not part of me” and she has neither married nor had children. ... She describes socializing with others as “boring” and has no interest in reading or watching entertainment about emotional issues or relationships.

In an earlier post on the Bickart article (More Friends on Facebook Does NOT Equal a Larger Amygdala), I noted that bigger is not always "better" (see Fig. 2 below):

One prominent example is the finding of larger amygdalae in children (and adults) with autism (Howard et al., 2000; Mosconi et al., 2009). However, the literature on this issue is variable (and voluminous)...² More consistent are observations of increased amygdala volumes in generalized anxiety disorder (Etkin et al., 2009; Schienle et al., 2010). In rats, chronic stress causes hypertrophy (enhanced dendritic arborization) of pyramidal and stellate neurons in the basolateral nucleus of the amygdala (Vyas et al., 2002).

Modified from Fig. 2 (Howard et al., 2000). Volume estimation of the amygdala by the stereological point counting method. Section area estimation of posterior, middle, and anterior amygdala sections, using a regular array of test points. Section areas are increased in autism compared to controls.

A further interpretive conundrum is presented by the variety of conditions that are associated with increased amygdala volume: first-episode patients with nonschizophrenic psychoses, women high in harm avoidance, learning disabled adolescents at high risk of schizophrenia, adopted Romanian adolescents who experienced severe early institutional deprivation, and political conservatism.³

Most of those things are not especially fantastic for an active social life...

Autism is often considered as a disorder of microcircuitry and of long-range connections, so determining the structural and functional connectivity of the amygdala with other brain regions is crucial. One view holds that "underconnectivity" is a characteristic feature of the brains of those with autism, although recently this hypothesis has been called into question.

A new study from Bickert and colleagues (2012) followed up on their previous morphometric work and examined the functional connectivity of the amydala in relation to offline social network size in a group of 30 young adults (19 of whom had been in their previous experiment). Two separate groups of subjects, a "discovery sample" (n=89) and a "replication sample" (n=83) were scanned with fMRI at rest to establish the large-scale amygdala networks related to social cognition.

In brief, three networks were identified: (1) the ventrolateral amygdala and "perception" network (connected with lateral orbitofrontal cortex); (2) the medial amygdala and "affiliation" network (connected with ventromedial prefrontal cortex); and (3) the dorsal amygdala and "aversion" network (connected with dorsal anterior cingulate cortex).














Figure 1 (Bickert et al., 2012). Hypothetical topographic model of amygdala subregions and their affiliated large-scale networks subserving social cognition. A schematic of (a) the amygdala subregions in coronal view that we hypothesize are anchors for (b) three large-scale networks subserving processes important for social cognition. Ins, insula; SS, somatosensory operculum; dTP, dorsal temporal pole; cACC, caudal anterior cingulate cortex; rACC, rostral anterior cingulate cortex; sgACC, ubgenual anterior cingulate cortex; MTL, medial temporal lobe; FG, fusiform gyrus; vTP, ventral temporal pole; vlSt, ventrolateral striatum; vmSt, ventromedial striatum.


In the experimental sample (n=30), stronger intrinsic connectivity within the "perception" and "affiliation" networks was correlated with larger real-life social networks, but connectivity within the "aversion" network was not. A thorough evaluation of the methods used to establish these relationships is beyond the scope of this post, but an important question remains: can the current results inform the patterns of amygdala connectivity observed in participants with autism?


Footnotes

¹ Although not specifically named, the participant was Gregory Blackstock, author of Blackstock's Collections: The Drawings of an Artistic Savant.

² In fact, recent meta-analyses suggest that individuals with ASD may have smaller amygdala volumes than controls (Cauda et al., 2011; Via et al., 2011). On the other hand, the literature on early childhood hypertrophy of the amygdala in autism seems consistent (Mosconi et al., 2009). But another study in adolescents and adults with Asperger syndrome observed larger amygdala volumes than in controls (Murphy et al., 2012).

³ This study was published in a newspaper, not in a peer reviewed journal (see Left Wing vs. Right Wing Brains).


References

Bickart, K., Hollenbeck, M., Barrett, L., & Dickerson, B. (2012). Intrinsic Amygdala-Cortical Functional Connectivity Predicts Social Network Size in Humans. Journal of Neuroscience, 32 (42), 14729-14741. DOI: 10.1523/JNEUROSCI.1599-12.2012

Bickart KC, Wright CI, Dautoff RJ, Dickerson BC, Barrett LF. (2011). Amygdala volume and social network size in humans. Nat Neurosci. 14:163-4.

Cauda F, Geda E, Sacco K, D'Agata F, Duca S, Geminiani G, Keller R. (2011). Greymatter abnormality in autism spectrum disorder: an activation likelihoodestimation meta-analysis study. J Neurol Neurosurg Psychiatry 82:1304-13.

J.R. Cooperrider, E.D. Bigler, J.S. Anderson, S. Doran, C. Ennis, N. Adluru, A.L. Alexander, A.L. Froehlich, M.B.D. Prigge, J.E. Lainhart. Dr. Temple Grandin: A neuropsychological and multimodal neuroimaging case study of a savant with autism. Program No. 18.08. 2012 Neuroscience Meeting Planner. New Orleans, LA: Society for Neuroscience, 2012. Online.

Corrigan, N., Richards, T., Treffert, D., & Dager, S. (2012). Toward a better understanding of the savant brain, Comprehensive Psychiatry, 53 (6), 706-717. DOI: 10.1016/j.comppsych.2011.11.006

Etkin A, Prater KE, Schatzberg AF, Menon V, Greicius MD. (2009). Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Arch Gen Psychiatry 66:1361-72.

Howard MA, Cowell PE, Boucher J, Broks P, Mayes A, Farrant A, Roberts N. (2000). Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism. Neuroreport 11:2931-5.

Kanai R, Bahrami B, Roylance R, Rees G. (2012). Online social network size isreflected in human brain structure. Proc Biol Sci. 279:1327-34.

Mosconi MW, Cody-Hazlett H, Poe MD, Gerig G, Gimpel-Smith R, Piven J. (2009). Longitudinal study of amygdala volume and joint attention in 2- to 4-year-old children with autism. Arch Gen Psychiatry 66:509-16.

Murphy CM, Deeley Q, Daly EM, Ecker C, O'Brien FM, Hallahan B, Loth E, Toal F, Reed S, Hales S, Robertson DM, Craig MC, Mullins D, Barker GJ, Lavender T, Johnston P, Murphy KC, Murphy DG. (2012). Anatomy and aging of the amygdala andhippocampus in autism spectrum disorder: an in vivo magnetic resonance imagingstudy of Asperger syndrome. Autism Res. 5:3-12.

Paré D, Quirk GJ, Ledoux JE. (2004). New vistas on amygdala networks in conditioned fear. J Neurophysiol. 92:1-9.

Phelps EA, LeDoux JE. (2005). Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175-87.

Schienle A, Ebner F, Schäfer A. (2010). Localized gray matter volume abnormalities in generalized anxiety disorder. Eur Arch Psychiatry Clin Neurosci. Sep 5. [Epub ahead of print].

Via E, Radua J, Cardoner N, Happé F, Mataix-Cols D. (2011). Meta-analysis of graymatter abnormalities in autism spectrum disorder: should Asperger disorder besubsumed under a broader umbrella of autistic spectrum disorder? Arch Gen Psychiatry 68:409-18.

Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci. 22:6810-8.