Olson IR, Plotzker A, Ezzyat Y. The Enigmatic temporal pole: a review of findings on social and emotional processing. Brain 130(Pt 7): 1718-1731

Center for Cognitive Neuroscience, University of Pennsylvania, 3720 Walnut Street, Room B51, Philadelphia, PA 19104-6196, USA.
Brain (Impact Factor: 9.2). 07/2007; 130(Pt 7):1718-31. DOI: 10.1093/brain/awm052
Source: PubMed


The function of the anterior-most portion of the temporal lobes, the temporal pole, is not well understood. Anatomists have long considered it part of an extended limbic system based on its location posterior to the orbital frontal cortex and lateral to the amygdala, along with its tight connectivity to limbic and paralimbic regions. Here we review the literature in both non-human primates and humans to assess the temporal pole's putative role in social and emotional processing. Reviewed findings indicate that it has some role in both social and emotional processes, including face recognition and theory of mind, that goes beyond semantic memory. We propose that the temporal pole binds complex, highly processed perceptual inputs to visceral emotional responses. Because perceptual inputs remain segregated into dorsal (auditory), medial (olfactory) and ventral (visual) streams, the integration of emotion with perception is channel specific.

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Available from: Ingrid R Olson, Oct 07, 2015
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    • "Men, on the other hand, showed higher RSFC to the temporal pole and vmPFC. The temporal pole has been suggested to be involved in the association of sensory input with emotional responses (Olson et al., 2007), while the connections between the amygdala and the vmPFC are critical in the acquisition of conditioned fear as well as in the extinction learning and extinction memory recall (Milad and Quirk, 2012). Our finding of enhanced LB amygdala-vmPFC connectivity in men relative to women is consistent with our recent data showing enhanced functional activation of the vmPFC in men relative to women during extinction recall (Lebron-Milad et al., 2012). "
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    ABSTRACT: The amygdala is a hub in emotional processing, including that of negative affect. Healthy men and women have distinct differences in amygdala responses, potentially setting the stage for the observed sex differences in the prevalence of fear, anxiety, and pain disorders. Here, we examined how amygdala subnuclei resting-state functional connectivity is affected by sex, as well as explored how the functional connectivity is related to estrogen levels. Resting-state functional connectivity was measured using functional magnetic resonance imaging (fMRI) with seeds placed in the left and right laterobasal (LB) and centromedial (CM) amygdala. Sex differences were studied in 48 healthy men and 48 healthy women, matched for age, while the association with estrogen was analyzed in a subsample of 24 women, for whom hormone levels had been assessed. For the hormone analyses, the subsample was further divided into a lower and higher estrogen levels group based on a median split. We found distinct sex differences in the LB and CM amygdala resting-state functional connectivity, as well as preliminary evidence for an association between estrogen levels and connectivity patterns. These results are potentially valuable in explaining why women are more afflicted by conditions of negative affect than are men, and could imply a mechanistic role for estrogen in modulating emotion.
    Psychoneuroendocrinology 09/2015; 63:34-42. DOI:10.1016/j.psyneuen.2015.09.012 · 4.94 Impact Factor
    • "These findings suggest that while the temporal lobes may be involved in explicit musical memory, their role in long-term musical memory processing may not be essential to maintain long-term representations of music. Furthermore the temporal lobe, and especially temporal pole areas, may be necessary to encode new musical memory, and once musical memories are encoded these areas might not be needed for memory retrieval (Olson et al., 2007; Jonides et al., 2008; Hsieh et al., 2011). This supports the suggestion of Baird and Samson (2009) that mostly implicit musical memory might be spared in Alzheimer's disease and thus our study gives a possible explanation for the preservation of long-term musical memory after severe bilateral temporal lobe damage (as in Alzheimer's disease), since we show that long-term musical memory representations heavily rely on ventral pre- SMA and the caudal anterior cingulate gyrus. "
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    ABSTRACT: Musical memory is considered to be partly independent from other memory systems. In Alzheimer's disease and different types of dementia, musical memory is surprisingly robust, and likewise for brain lesions affecting other kinds of memory. However, the mechanisms and neural substrates of musical memory remain poorly understood. In a group of 32 normal young human subjects (16 male and 16 female, mean age of 28.0 ± 2.2 years), we performed a 7 T functional magnetic resonance imaging study of brain responses to music excerpts that were unknown, recently known (heard an hour before scanning), and long-known. We used multivariate pattern classification to identify brain regions that encode long-term musical memory. The results showed a crucial role for the caudal anterior cingulate and the ventral pre-supplementary motor area in the neural encoding of long-known as compared with recently known and unknown music. In the second part of the study, we analysed data of three essential Alzheimer's disease biomarkers in a region of interest derived from our musical memory findings (caudal anterior cingulate cortex and ventral pre-supplementary motor area) in 20 patients with Alzheimer's disease (10 male and 10 female, mean age of 68.9 ± 9.0 years) and 34 healthy control subjects (14 male and 20 female, mean age of 68.1 ± 7.2 years). Interestingly, the regions identified to encode musical memory corresponded to areas that showed substantially minimal cortical atrophy (as measured with magnetic resonance imaging), and minimal disruption of glucose-metabolism (as measured with (18)F-fluorodeoxyglucose positron emission tomography), as compared to the rest of the brain. However, amyloid-β deposition (as measured with (18)F-flobetapir positron emission tomography) within the currently observed regions of interest was not substantially less than in the rest of the brain, which suggests that the regions of interest were still in a very early stage of the expected course of biomarker development in these regions (amyloid accumulation → hypometabolism → cortical atrophy) and therefore relatively well preserved. Given the observed overlap of musical memory regions with areas that are relatively spared in Alzheimer's disease, the current findings may thus explain the surprising preservation of musical memory in this neurodegenerative disease. © The Author (2015). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email:
    Brain 06/2015; 138(Pt 8). DOI:10.1093/brain/awv135 · 9.20 Impact Factor
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    • "Many researchers have noted that the ATLs are involved in social cognition in humans and primates (Kluver and Bucy 1937; Edwards-Lee et al. 1997; Frith and Frith 2003; Gallate et al. 2011). More recently, several research groups have proposed that part or all of the ATL codes social concepts, including person knowledge and emotional concepts (Thompson et al. 2003; Olson et al. 2007; Zahn et al. 2007, 2009; Ross and Olson 2010; Olson et al. 2013). Deficits in social behavior are often observed in SD patients, including social awkwardness, person recognition deficits, and a loss of empathy (Thompson et al. 2003; Chan et al. 2009). "
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    ABSTRACT: The roles of the right and left anterior temporal lobes (ATLs) in conceptual knowledge are a source of debate between 4 conflicting accounts. Possible ATL specializations include: (1) Processing of verbal versus non-verbal inputs; (2) the involvement of word retrieval; and (3) the social content of the stimuli. Conversely, the "hub-and-spoke" account holds that both ATLs form a bilateral functionally unified system. Using activation likelihood estimation (ALE) to compare the probability of left and right ATL activation, we analyzed 97 functional neuroimaging studies of conceptual knowledge, organized according to the predictions of the three specialized hypotheses. The primary result was that ATL activation was predominately bilateral and highly overlapping for all stimulus types. Secondary to this bilateral representation, there were subtle gradations both between and within the ATLs. Activations were more likely to be left lateralized when the input was a written word or when word retrieval was required. These data are best accommodated by a graded version of the hub-and-spoke account, whereby representation of conceptual knowledge is supported through bilateral yet graded connectivity between the ATLs and various modality-specific sensory, motor, and limbic cortices. © The Author 2015. Published by Oxford University Press.
    Cerebral Cortex 03/2015; DOI:10.1093/cercor/bhv024 · 8.67 Impact Factor
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