Neural inhibition enables selection during language processing

Abstract

Whether grocery shopping or choosing words to express a thought, selecting between options can be challenging, especially for people with anxiety. We investigate the neural mechanisms supporting selection during language processing and its breakdown in anxiety.Our neural network simulations demonstrate a critical role for competitive, inhibitory dynamics supported by GABAergic interneurons. As predicted by our model, we find that anxiety (associated with reduced neural inhibition) impairs selection among options and associated prefrontal cortical activity, even in a simple, nonaffective verb-generation task, and the GABA agonist midazolam (which increases neural inhibition) improves selection, whereas retrieval from semantic memory is unaffected when selection demands are low. Neural inhibition is key to choosing our words.P eople claim to love the freedom of unlimited choices, but in reality we are often stymied by too many options and disconcerted by not knowing what the outcomes of our choices will be. Selecting among multiple options is effortful and time consuming, whether choosing among fruit jams (1), retirement plans (2), or medical treatments (3). This problem is particularly pervasive during language production, when we must constantly choose words to express a thought (4-6). People with anxiety disorders find coping with too many options particularly difficult, and struggle with decision-making problems (7), indecisiveness (8), and intolerance of uncertainty (9). What mechanisms allow us to select among multiple options when speaking, and why does this process break down in people with anxiety? Current psychological theories of selection focus on the importance of cognitive control (5) and prefrontal cortical regions (4, 6, 10), but do not address questions at the level of specific neural mechanisms. We address these questions by implementing a unified, biologically plausible computational model of selection, and testing its predictions about both brain and behavior in humans making choices in a well-controlled language production task.Our model demonstrates how competitive, inhibitory dynamics among neurons in prefrontal cortical networks (11) support selection between alternatives. Specifically, these competitive dynamics serve to sharpen cognitive representations by amplifying activity in the most active, task-relevant, representations (e.g., the most appropriate word to complete a sentence) and suppressing competing representations (e.g., for the many other word possibilities). A tenet of the model is that these critical dynamics occur via inhibitory, GABAergic interneurons (12-14). Here we test the predictions of the model regarding selection processes that are supported by the left ventrolateral prefrontal cortex. We do so for the following reasons: (i) this region has been implicated in selecting among competing alternatives during language processing (6, 15-18); (ii) this region shows altered activity in individuals who suffer from anxiety (particularly anxious apprehension, characterized by w...

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“…Planum temporal forms the heart of Wernicke's area and besides ϭϳ being involved in the processing of language has also been implicated in auditory spatial processing. A recent fMRI study demonstrated that anxiety being associated with reduced neural inhibition impairs selection between options and associated prefrontal cortical activity during selection and retrieval of words from semantic memory with a verb generation task (Snyder et al, 2010). The authors of the study focussed on the relation between anxiety and the activity specifically in left ventrolateral prefrontal cortex (VLPFC).…”