Impaired Facilitatory Mechanisms of Auditory Attention After Damage of the Lateral Prefrontal Cortex

Abstract

There is growing evidence that auditory selective attention operates via distinct facilitatory and inhibitory mechanisms enabling selective enhancement and suppression of sound processing, respectively. The lateral prefrontal cortex (LPFC) plays a crucial role in the top-down control of selective attention. However, whether the LPFC controls facilitatory, inhibitory, or both attentional mechanisms is unclear. Facilitatory and inhibitory mechanisms were assessed, in patients with LPFC damage, by comparing event-related potentials (ERPs) to attended and ignored sounds with ERPs to these same sounds when attention was equally distributed to all sounds. In control subjects, we observed 2 late frontally distributed ERP components: a transient facilitatory component occurring from 150 to 250 ms after sound onset; and an inhibitory component onsetting at 250 ms. Only the facilitatory component was affected in patients with LPFC damage: this component was absent when attending to sounds delivered in the ear contralateral to the lesion, with the most prominent decreases observed over the damaged brain regions. These findings have 2 important implications: (i) they provide evidence for functionally distinct facilitatory and inhibitory mechanisms supporting late auditory selective attention; (ii) they show that the LPFC is involved in the control of the facilitatory mechanisms of auditory attention.

Insights into Human Behavior from Lesions to the Prefrontal Cortex

“…These decreased extrastriate neural responses were accompanied by impairments in the ability to detect targets presented in the contralesional visual field. Diminished neural responses have been similarly reported in DLPFC patients during selective auditory attention (Bidet-Caulet et al, 2014). These studies suggest that the DLPFC plays an important role in attention by providing top-down facilitatory input to sensory cortices.…”

The Dorsolateral Prefrontal Cortex in Acute and Chronic Pain

“…However, it has also been shown to be involved in cognitive processes 18, 43, 62, 96 , such as attention 6, 104–106 , value encoding 11, 40, 46, 53, 95 , working memory 5 , creativity 52 , decision-making 71, 73 , and emotional regulation 15, 27, 29, 67, 99 .…”

Correlates of auditory decision making in prefrontal, auditory, and basal lateral amygdala cortical areas

“…Both prefrontal (Green, Doesburg et al 2011, Bidet-Caulet, Buchanan et al 2015 and parietal (Michalka, Rosen et al 2016, Deng, Reinhart et al 2019, Deng, Choi et al 2020) cortex have been shown to play important roles in auditory spatial attention in humans. Although we found clear responses related to the cued side in dlPFC, they followed AC.…”

“…Spatial selective listening is critical for solving everyday problems including the "cocktail party problem", which requires attending to one sound source amidst a noisy background of competing sources (Cherry 1953). Common auditory spatial selective listening paradigms in research with humans include modified Posner paradigms in which subjects have to detect auditory stimuli after being cued to a spatial location (Spence and Driver 1994, Alho, Medvedev et al 1999, McDonald and Ward 1999, Mayer, Harrington et al 2007, Mayer, Mannell et al 2009, Roberts, Summerfield et al 2009, Teshiba, Ling et al 2013) and selective listening studies (Ahveninen, Huang et al 2013, Frey, Mainy et al 2014, Bidet-Caulet, Buchanan et al 2015.…”

“…Previous work in humans has shown that auditory cortex (AC) plays an important role in spatial selective listening tasks, through interactions with prefrontal (Alho, Medvedev et al 1999) and parietal (Deng, Reinhart et al 2019) cortex, as well as auditory perceptual decision making (Tsunada, Liu et al 2016, Christison-Lagay andCohen 2018). In humans with dorsal lateral prefrontal cortex (dlPFC) damage, studies of selective listening found decreases in a facilitatory evoked activity component, recorded over dlFPC (Bidet-Caulet, Buchanan et al 2015), and other work has shown that dlPFC supports important aspects of auditory working memory (Plakke, Hwang et al 2015). It has also been suggested that the basal lateral amygdala (BLA) contributes to attention and value based decision making, in the visual domain, by encoding information about spatial location and the motivational significance of stimuli Salzman 2014, Costa, Mitz et al 2019).…”