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Temporopolar regions of the human brain

Journal

BRAIN
Volume 146, Issue 1, Pages 20-41

Publisher

OXFORD UNIV PRESS
DOI: 10.1093/brain/awac339

Keywords

temporal pole; semantics; word comprehension; object recognition; dementia; aphasia; TDP-C

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This article reviews the temporopolar region, which was once considered unknown territory but has now emerged as a crucial intersection for the development of word meaning, object recognition, and social conduct. The function of the temporopolar region is closely related to cognition and behavior, but its function is impaired in neurodegenerative diseases. The left temporopolar region is crucial for language comprehension, while behavioral control and non-verbal object recognition show bilateral representation. The temporopolar region is also associated with auditory, visual, and limbic processing. The neural matrix in this region supports the transformation of object and word representations from unimodal percepts to multimodal concepts. Dysfunction in the temporopolar region can lead to category blurring and comprehension impairments.
Mesulam reviews the temporopolar region, an area once considered terra incognita that has since emerged as a crucial crossroads for the associative elaboration of word meaning, object recognition and social conduct. Following prolonged neglect during the formative decades of behavioural neurology, the temporopolar region has become a site of vibrant research on the neurobiology of cognition and conduct. This turnaround can be attributed to increasing recognition of neurodegenerative diseases that target temporopolar regions for peak destruction. The resultant syndromes include behavioural dementia, associative agnosia, semantic forms of primary progressive aphasia and semantic dementia. Clinicopathological correlations show that object naming and word comprehension are critically dependent on the language-dominant (usually left) temporopolar region, whereas behavioural control and non-verbal object recognition display a more bilateral representation with a rightward bias. Neuroanatomical experiments in macaques and neuroimaging in humans show that the temporoparietal region sits at the confluence of auditory, visual and limbic streams of processing at the downstream (deep) pole of the 'what' pathway. The functional neuroanatomy of this region revolves around three axes, an anterograde horizontal axis from unimodal to heteromodal and paralimbic cortex; a radial axis where visual (ventral), auditory (dorsal) and paralimbic (medial) territories encircle temporopolar cortex and display hemispheric asymmetry; and a vertical depth-of-processing axis for the associative elaboration of words, objects and interoceptive states. One function of this neural matrix is to support the transformation of object and word representations from unimodal percepts to multimodal concepts. The underlying process is likely to start at canonical gateways that successively lead to generic (superordinate), specific (basic) and unique levels of recognition. A first sign of left temporopolar dysfunction takes the form of taxonomic blurring where boundaries among categories are preserved but not boundaries among exemplars of a category. Semantic paraphasias and coordinate errors in word-picture verification tests are consequences of this phenomenon. Eventually, boundaries among categories are also blurred and comprehension impairments become more profound. The medial temporopolar region belongs to the amygdalocentric component of the limbic system and stands to integrate exteroceptive information with interoceptive states underlying social interactions. Review of the pertinent literature shows that word comprehension and conduct impairments caused by temporopolar strokes and temporal lobectomy are far less severe than those seen in temporopolar atrophies. One explanation for this unexpected discrepancy invokes the miswiring of residual temporopolar neurons during the many years of indolently progressive neurodegeneration. According to this hypothesis, the temporopolar regions become not only dysfunctional but also sources of aberrant outputs that interfere with the function of areas elsewhere in the language and paralimbic networks, a juxtaposition not seen in lobectomy or stroke.

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