Spoken Word Memory Traces within the Human Auditory Cortex Revealed by Repetition Priming and Functional Magnetic Resonance Imaging

Abstract

Previous neuroimaging studies in the visual domain have shown that neurons along the perceptual processing pathway retain the physical properties of written words, faces, and objects. The aim of this study was to reveal the existence of similar neuronal properties within the human auditory cortex. Brain activity was measured using functional magnetic resonance imaging during a repetition priming paradigm, with words and pseudowords heard in an acoustically degraded format. Both the amplitude and peak latency of the hemodynamic response (HR) were assessed to determine the nature of the neuronal signature of spoken word priming. A statistically significant stimulus type by repetition interaction was found in various bilateral auditory cortical areas, demonstrating either HR suppression and enhancement for repeated spoken words and pseudowords, respectively, or word-specific repetition suppression without any significant effects for pseudowords. Repetition latency shift only occurred with word-specific repetition suppression in the right middle/posterior superior temporal sulcus. In this region, both repetition suppression and latency shift were related to behavioral priming. Our findings highlight for the first time the existence of long-term spoken word memory traces within the human auditory cortex. The timescale of auditory information integration and the neuronal mechanisms underlying priming both appear to differ according to the level of representations coded by neurons. Repetition may "sharpen" word-nonspecific representations coding short temporal variations, whereas a complex interaction between the activation strength and temporal integration of neuronal activity may occur in neuronal populations coding word-specific representations within longer temporal windows.

fMRI Syntactic and Lexical Repetition Effects Reveal the Initial Stages of Learning a New Language

“…3). This pattern of effects ties in with similar dissociations that have been found to the repetition of pseudowords compared with words (Fiebach et al, 2005;Gagnepain et al, 2008), suggesting that the RE effects might be related to the building of new representations for these novel word orders. The infrequent novel structure was particularly sensitive to repetition (its RE effect was significantly different from zero and there was a trend toward a stronger effect compared with the frequent structures).…”

“…In neuroimaging experiments, there is a contrast between repetition effects to known items (from objects to words to syntactic structures), which results in a reduction in activation: repetition suppression (RS), and repetition effects to novel items (eg, unknown objects, pseudowords), where repetition is accompanied by an increase in activation (Henson et al, 2000;Gagnepain et al, 2008): repetition enhancement (RE). Whereas RS is thought to reflect the facilitation of processing within or the sharpening of an existing neural representation, RE in the context of novel item repetition has been linked to the formation of neural representations (Grill-Spector et al, 2006; Segaert et al, 2013).…”

Predictive processing increases intelligibility of acoustically distorted speech: Behavioral and neural correlates

“…In this way, word‐specific memory templates could serve as a rapid adaptive filter that increases speech intelligibility in suboptimal listening conditions. While previous studies have linked decreased BOLD‐responses with shorter response times for making decisions about the stimuli (Gagnepain et al., 2008), our study suggests that in suboptimal conditions the behavioral benefit of the neural mechanisms underlying BOLD‐suppression might be increased speech intelligibility. Further analyses, for example using Dynamic Causal Modeling (Tuennerhoff & Noppeney, 2016), would be needed to establish whether the decreases in the activity in auditory cortex reflect bottom‐up (e.g., local sparse coding through representation sharpening) or top‐down (e.g., predictive coding) processing, or whether both mechanisms are involved.…”

“…This proposes that neurons coding word‐specific information send inhibitory feedback to the neurons coding features that are not essential for word identification, and that this results in a sparser and more specific neural representation of the word (Grill‐Spector et al., 2006; Henson, 2003; Wiggs & Martin, 1998). Further, these word‐specific memory representations might encode invariant global acoustic features of a word formulated as an average of the exposures to the various acoustic forms of that word during the subject's lifespan (Gagnepain et al., 2008). In this way, word‐specific memory templates could serve as a rapid adaptive filter that increases speech intelligibility in suboptimal listening conditions.…”

Where sound position influences sound object representations: A 7-T fMRI study

“…Multiple levels of representation are likely to exist also for other auditory features, such as the physical properties of the sound track or stimulus familiarity, as recently indicated by fMRI priming studies (De Lucia et al, 2009). The behavioural priming effect, i.e., shorter reaction times, has been reported for words, independently of whether they were repeated by the same or a different speaker (Gagnepain et al, 2008;Orfanidou et al, 2006). The priming suppression of the BOLD response and shorter response latency occurred, however, differentially in different parts of the temporal regions, suggesting the coexistence of speaker-dependent and speaker-invariant auditory word representations.…”