Left Anterior Temporal Lobe and Bilateral Anterior Cingulate Cortex Are Semantic Hub Regions: Evidence from Behavior-Nodal Degree Mapping in Brain-Damaged Patients

Abstract

The organizational principles of semantic memory in the human brain are still controversial. Although studies have shown that the semantic system contains hub regions that bind information from different sensorimotoric modalities to form concepts, it is unknown whether there are hub regions other than the anterior temporal lobe (ATL). Meanwhile, previous studies have rarely used network measurements to explore the hubs or correlated network indexes with semantic performance, although the most direct supportive evidence of hubs should come from the network perspective. To fill this gap, we correlated the brain-network index with semantic performance in 86 brain-damaged patients. We especially selected the nodal degree measure that reflects how well a node is connected in the network. The measure was calculated as the total number of connections of a given node with other nodes in the resting-state functional MRI network. Semantic ability was measured using the performance of both general and modality-specific (object form, color, motion, sound, manipulation, and function) semantic tasks. We found that the left ATL and the bilateral anterior cingulate cortex could be semantic hubs because the reduced nodal degree values of these regions could effectively predict the deficits in both general and modality-specific semantic performance. Moreover, the effects remained when the analyses were performed only in the patients who did not have lesions in these regions. The two hub regions might support semantic representations and executive control processes, respectively. These data provide empirical evidence for the distributed-plus-hub theory of semantic memory from the network perspective.

Human Cortical Neurons in the Anterior Temporal Lobe Reinstate Spiking Activity during Verbal Memory Retrieval

“…Our results provide direct evidence that successfully retrieving associations between words involves reinstatement of population spiking activity in the MTG, a brain region previously highlighted for its role in semantic processing [9–11]. Prior work investigating cortical reinstatement has relied on correlates of neural activity such as fMRI BOLD and iEEG oscillatory activity [4–6, 15].…”

“…Recent advances using high density microelectrode arrays (MEAs) have allowed clinicians to record from populations of neurons in the human cortex [7,8]. Here we use MEAs to record neuronal spiking activity in the human middle temporal gyrus (MTG), a cortical region supporting the semantic representation of words [9–11], as participants performed a verbal paired associates task. We provide novel evidence that population spiking activity in the MTG form distinct representations of semantic concepts, and that these representations are reinstated during the retrieval of those words.…”

Revealing the Dynamic Modulations That Underpin a Resilient Neural Network for Semantic Cognition: An fMRI Investigation in Patients With Anterior Temporal Lobe Resection

“…This mild semantic impairment is shown through slower response times on semantic tasks (e.g., picture naming, word-picture matching, synonym judgment), rather than marked decreases in accuracy ( Wilkins and Moscovitch 1978 ; Lambon Ralph et al 2012 ; Rice et al 2018 ), although on more challenging/specific level semantic concepts decreases in accuracy performance are found. This mild semantic impairment in patients with unilateral ATL resection is in contrast to the severe semantic impairment shown after bilateral ATL damage/resection ( Terzian and Ore 1955 ; Lambon Ralph et al 2010 , 2012 ; Mion et al 2010 ; Zhao et al 2017 ). This pattern of results was also shown in seminal nonhuman primate work ( Brown and Schafer 1888 ; Kluver and Bucy 1937 , 1938 ), in which unilateral resection resulted in transient deficits, whereas bilateral resection resulted in severe multimodal semantic and episodic memory impairments.…”

Morphometric correlates of anomia in patients with small left temporopolar lesions

“…This view highlights the interdependency between conceptual representations and word retrieval processes (Lambon Ralph, McClelland, Patterson, Galton, & Hodges, ; Riès et al ., ). Thus, the significant effect observed in the left ACC could be interpreted as a contribution to executive control processes (Riès et al ., ; Zhao et al ., ). This region has been included in a network of frontal regions associated with word selection in picture naming and verbal fluency tasks (Fu et al ., ; Riès, Karzmark, Navarrete, Knight, & Dronkers, ; for a review see Price, ), and also in selection processes in non‐language production tasks (Riès et al ., ).…”