Triangulation of the neurocomputational architecture underpinning reading aloud

Abstract

The goal of cognitive neuroscience is to integrate cognitive models with knowledge about underlying neural machinery. This significant challenge was explored in relation to word reading, where sophisticated computational-cognitive models exist but have made limited contact with neural data. Using distortion-corrected functional MRI and dynamic causal modeling, we investigated the interactions between brain regions dedicated to orthographic, semantic, and phonological processing while participants read words aloud. We found that the lateral anterior temporal lobe exhibited increased activation when participants read words with irregular spellings. This area is implicated in semantic processing but has not previously been considered part of the reading network. We also found meaningful individual differences in the activation of this region: Activity was predicted by an independent measure of the degree to which participants use semantic knowledge to read. These characteristics are predicted by the connectionist Triangle Model of reading and indicate a key role for semantic knowledge in reading aloud. Premotor regions associated with phonological processing displayed the reverse characteristics. Changes in the functional connectivity of the reading network during irregular word reading also were consistent with semantic recruitment. These data support the view that reading aloud is underpinned by the joint operation of two neural pathways. They reveal that (i) the ATL is an important element of the ventral semantic pathway and (ii) the division of labor between the two routes varies according to both the properties of the words being read and individual differences in the degree to which participants rely on each route.triangle model | anterior temporal lobe | semantic reliance | reading | surface dyslexia C ognitive neuroscience offers the exciting prospect of understanding the neural basis of cognitive behaviors, a goal which requires integration of sophisticated cognitive models with knowledge about the underlying neural machinery. As a key cognitive skill, reading provides an advanced test case. Computationally implemented theories present detailed accounts of how reading is accomplished at a cognitive level (1-4). To achieve a full understanding of reading and its impairment in neurological disorders, these cognitive theories must be integrated with information about the neural basis of the reading system. However, although various studies have explored the neural basis of reading (5), the level of integration between cognitive and neural models remains limited. In the present study, we used an improved functional MRI (fMRI) protocol to test the specific predictions of an influential computational model of word reading: the connectionist "Triangle Model" (2). We were able to map specific elements of this cognitive model onto different cortical regions, thereby providing a direct link between cognitive theorizing and neural implementation. Specifically, we provide insights into the division of labor between se...

Reading words and other people: A comparison of exception word, familiar face and affect processing in the left and right temporal variants of primary progressive aphasia

“…A. Wilson et al, 2012; Woollams et al, 2007). This conforms with a recent proposal that the left lateral temporal neocortex plays an intermediary role in mapping between ventrally-situated transmodal conceptual knowledge representation and the frontal speech production network, subtending lexico-semantic processes such as reading and naming (Hoffman et al, 2015; Mehta et al, in press). However, the present study highlights a mid portion of the middle temporal gyrus that is considerably more posterior than the typical area of atrophy observed in svPPA and the region implicated in prior imaging studies of reading.…”

“…Our results are indicative of a critical role of the left-hemisphere lateral temporal cortex in exception word reading and are consistent with prior neuropsychological, computational modeling and functional imaging studies (Brambati, Ogar, Neuhaus, Miller, & Gorno-Tempini, 2009; Henry, Beeson, Alexander, & Rapcsak, 2012; Hoffman et al, 2015; Ueno, Saito, Rogers, & Lambon Ralph, 2011; M. A. Wilson et al, 2012; Woollams et al, 2007).…”

“…Two recent fMRI studies demonstrated increased activation of the left lateral temporal cortex for reading exception words compared to regular words (Hoffman et al, 2015) and pseudowords (M. A. Wilson et al, 2012), but in an anterior portion of the MTG close to the polar cortex.…”

“…The cortical region implicated in semantic cognition and language over the course of svPPA, however, extends to include much of the rostral half of the temporal lobe (Nestor et al, 2006). Moreover, correlations between semantic dysfunction and hypometabolism in svPPA as well as functional neuroimaging studies are now implicating regions caudal to the temporal pole, including lateral and ventrolateral temporal lobe neocortex (Binney, Embleton, Jefferies, Parker, & Lambon Ralph, 2010; Hoffman, Lambon Ralph, & Woollams, 2015; Mion et al, 2010). The VOIs used in the present study were defined solely for the purpose of grossly examining the distribution of atrophy in the patient groups along an anatomically-defined rostral-caudal axis of the temporal lobe and without particular concern regarding more specific functional definitions of what constitutes the ATL.…”

Dough, tough, cough, rough: A “fast” fMRI localizer of component processes in reading

“…From the VWFA, the ventral system extends into middle and inferior temporal gyrus (Tagamets, Novick, Chalmers, & Friedman, 2000), both of which have been linked to semantic processing (Fiebach et al, 2002; Simos et al, 2002). In addition, recent evidence has shown that the anterior temporal lobe (ATL) could also be an important semantic site in this pathway (Hoffman, Ralph, & Woollams, 2015). …”