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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

ABSTRACT

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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    • "Our neuroimaging and behavioural findings support the view that involvement of the right anterior temporal lobe is responsible for the emergence of social cognition deficits in these patients (see alsoIrish et al., 2014). The functions of the right temporal lobeDownloaded from continue to be somewhat elusive to neuroscientists (Olson et al., 2007Olson et al., , 2013), with its primary role still contentious (Gainotti, 2015). Some argue that this region is necessary for representation of non-verbal information (with verbal information primarily subserved by the left temporal lobe), whilst others have suggested that the right temporal lobe is specialized for social cognition (for review of these arguments seeGainotti, 2015). "
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    ABSTRACT: The typical presentation of semantic dementia is associated with marked, left predominant anterior temporal lobe atrophy and with changes in language. About 30% of individuals, however, present with predominant right anterior temporal lobe atrophy, usually accompanied by behavioural changes and prosopagnosia. Here, we aimed to establish whether these initially distinct clinical presentations evolve into a similar syndrome at the neural and behavioural level. Thirty-one patients who presented with predominant anterior temporal lobe atrophy were included. Based on imaging, patients were categorized as either predominant left (n = 22) or right (n = 9) semantic dementia. Thirty-three Alzheimer's disease patients and 25 healthy controls were included for comparison. Participants completed the Addenbrooke's Cognitive Examination, a Face and Emotion Processing Battery and the Cambridge Behavioural Inventory, and underwent magnetic resonance imaging annually. Longitudinal neuroimaging analyses showed greater right temporal pole atrophy in left semantic dementia than Alzheimer's disease, whereas right semantic dementia showed greater orbitofrontal and left temporal lobe atrophy than Alzheimer's disease. Importantly, direct comparisons between semantic dementia groups revealed that over time, left semantic dementia showed progressive thinning in the right temporal pole, whereas right semantic dementia showed thinning in the orbitofrontal cortex and anterior cingulate. Behaviourally, longitudinal analyses revealed that general cognition declined in all patients. In contrast, patients with left and right semantic dementia showed greater emotion recognition decline than Alzheimer's disease. In addition, left semantic dementia showed greater motivation loss than Alzheimer's disease. Correlational analyses revealed that emotion recognition was associated with right temporal pole, right medial orbitofrontal and right fusiform integrity, while changes in motivation were associated with right temporal pole cortical thinning. While left and right semantic dementia show distinct profiles at presentation, both phenotypes develop deficits in emotion recognition and behaviour. These findings highlight the pervasive socio-emotional deficits in frontotemporal dementia, even in patients with an initial language presentation. These changes reflect right anterior temporal and orbitofrontal cortex degeneration, underscoring the role of these regions in social cognition and behaviour.
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    • "The temporal lobe pole plays a not yet completely but probably important role in the central processing of olfactory information. A role of the temporal lobe was seen as " linking odor object representations to transmodal networks, given its anatomical proximity to olfactory and visual object processing areas " (Kasai et al., 2003;Olofsson et al., 2013;Olson et al., 2007). Lesions induced by radiation have been found to be associated with decreased olfactory function (Leyrer et al., 2014)and deficits of the temporal lobe pole in primary progressive aphasia were related to severe deficits in odor naming and matching, which would be a compatible association provided the hypothesis that distorted input from a damaged lateral orbitofrontal cortex results in the report of a wrong percep- tion. "
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    ABSTRACT: The presence of cerebral lesions in patients with neurosensory alterations provides a unique window into brain function. Using a fuzzy logic based combination of morphological information about 27 olfactory-eloquent brain regions acquired with four different brain imaging techniques, patterns of brain damage were analyzed in 127 patients who displayed anosmia, i.e., complete loss of the sense of smell (n = 81), or other and mechanistically still incompletely understood olfactory dysfunctions including parosmia, i.e., distorted perceptions of olfactory stimuli (n = 50), or phantosmia, i.e., olfactory hallucinations (n = 22). A higher prevalence of parosmia, and as a tendency also phantosmia, was observed in subjects with medium overall brain damage. Further analysis showed a lower frequency of lesions in the right temporal lobe in patients with parosmia than in patients without parosmia. This negative direction of the differences was unique for parosmia. In anosmia, and also in phantosmia, lesions were more frequent in patients displaying the respective symptoms than in those without these dysfunctions. In anosmic patients, lesions in the right olfactory bulb region were much more frequent than in patients with preserved sense of smell, whereas a higher frequency of carriers of lesions in the left frontal lobe was observed for phantosmia. We conclude that anosmia, and phantosmia, are the result of lost function in relevant brain areas whereas parosmia is more complex, requiring damaged and intact brain regions at the same time.
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    • "Consistent with this notion, activation within visual sensory, temporal, and parietal regions implicated in social-affective processing was also greater among younger adolescents during reappraisal. This included both regions implicated in the encoding of perceptual features of social stimuli (fusiform gyrus, inferior occipital)[Gauthier et al., 2000;Haxby et al., 2002]and also those involved in social perception, including thinking about another's mental state (superior temporal sulcus, lateral temporal regions, angular gyrus, and the temporal poles)[Allison et al., 2000;Olson et al., 2007;Van Overwalle and Baetens, 2009;Vigneau et al., 2006;Young et al., 2010]. Importantly, recent work has indicated that temporal cortical regions, as identified in our age-related analysis , might be particularly important to transformations of stimulus meaning that enable emotional change[Buhle et al., 2014;Ochsner et al., 2012]. "
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    ABSTRACT: Few studies have examined the neural correlates of emotion regulation across adolescence and young adulthood. Existing studies of cognitive reappraisal indicate that improvements in regulatory efficiency may develop linearly across this period, in accordance with maturation of prefrontal cortical systems. However, there is also evidence for adolescent differences in reappraisal specific to the activation of "social-information processing network" regions, including the amygdala and temporal-occipital cortices. Here, we use fMRI to examine the neural correlates of emotional reactivity and reappraisal in response to aversive social imagery in a group of 78 adolescents and young adults aged 15-25 years. Within the group, younger participants exhibited greater activation of temporal-occipital brain regions during reappraisal in combination with weaker suppression of amygdala reactivity-the latter being a general correlate of successful reappraisal. Further analyses demonstrated that these age-related influences on amygdala reactivity were specifically mediated by activation of the fusiform face area. Overall, these findings suggest that enhanced processing of salient social cues (i.e., faces) increases reactivity of the amygdala during reappraisal and that this relationship is stronger in younger adolescents. How these relationships contribute to well-known vulnerabilities of emotion regulation during this developmental period will be an important topic for ongoing research. Hum Brain Mapp, 2015. © 2015 Wiley Periodicals, Inc.
    No preview · Article · Nov 2015 · Human Brain Mapping
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