Priming production: Neural evidence for enhanced automatic semantic activity preceding language production in schizophrenia

Abstract

Introduction: Lexico-semantic disturbances are considered central to schizophrenia. Clinically, their clearest manifestation is in language production. However, most studies probing their underlying mechanisms have used comprehension or categorization tasks. Here, we probed automatic semantic activity prior to language production in schizophrenia using event-related potentials (ERPs).

Methods: 19 people with schizophrenia and 16 demographically-matched healthy controls named target pictures that were very quickly preceded by masked prime words. To probe automatic semantic activity prior to production, we measured the N400 ERP component evoked by these targets. To determine the origin of any automatic semantic abnormalities, we manipulated the type of relationship between prime and target such that they overlapped in (a) their semantic features (semantically related, e.g. "cake" preceding a < picture of a pie >, (b) their initial phonemes (phonemically related, e.g. "stomach" preceding a < picture of a starfish >), or (c) both their semantic features and their orthographic/phonological word form (identity related, e.g. "socks" preceding a < picture of socks >). For each of these three types of relationship, the same targets were paired with unrelated prime words (counterbalanced across lists). We contrasted ERPs and naming times to each type of related target with its corresponding unrelated target.

Results: People with schizophrenia showed abnormal N400 modulation prior to naming identity related (versus unrelated) targets: whereas healthy control participants produced a smaller amplitude N400 to identity related than unrelated targets, patients showed the opposite pattern, producing a larger N400 to identity related than unrelated targets. This abnormality was specific to the identity related targets. Just like healthy control participants, people with schizophrenia produced a smaller N400 to semantically related than to unrelated targets, and showed no difference in the N400 evoked by phonemically related and unrelated targets. There were no differences between the two groups in the pattern of naming times across conditions.

Conclusion: People with schizophrenia can show abnormal neural activity associated with automatic semantic processing prior to language production. The specificity of this abnormality to the identity related targets suggests that that, rather than arising from abnormalities of either semantic features or lexical form alone, it may stem from disruptions of mappings (connections) between the meaning of words and their form.

Keywords: ERP; Language production; N400; Picture word interference; Prediction; Thought disorder.

Fig. 1

Example of word-picture stimuli pairs. Stimuli consisted of a prime word that was related to a target picture along one of three types of relationships: Semantic, Phonemic Onset, or Identity. For each Relationship Type, an Unrelated prime word was paired with the same picture. The average length, number of syllables, number of phonemes and frequencies of the names of the target pictures are given, with standard deviations in parentheses. Values were taken from the English Lexicon Project, http://elexicon.wustl.edu/. The pictures were presented in color and were taken from the Hemera Photo Objects database (Hemera Technologies Inc., 2002). There was no significant difference in log frequency (F(2, 263) = 0.066, p = 0.936), number of letters ((2, 263) = 0.886, p = 0.414), number of phonemes (F(2, 263) = 0.737, p = 0.479), or number of syllables (F(2, 263) = 1.205, p = 0.301) of the names of target pictures across the three Relationship Types. The pictures were also matched across the three Relationship Types on familiarity (values taken from the MRC Database and available for 73% of the target pictures used), (F(2, 194) = 1.129, p > 0.325).

Fig. 2

Trial Presentation. Each trial consisted of a fixation prompt, a forward mask, a briefly-presented content word, and a picture. The picture stayed on the screen until participants named the item (with a soft limit of approximately 2 s).

Fig. 3

Naming times in the control and schizophrenia groups. Naming times were calculated as the time from the onset of correctly-named target pictures until the onset of the verbal response (excluding disfluencies like “um”). Black horizontal lines in each box indicate the median naming time across all trials of that condition from all participants in each participant group, with a notch indicating a 95% confidence interval for the median. The top and bottom box boundaries indicate the 3rd and 1st quartiles, respectively.

Fig. 4

Grand-averaged waveforms in the control and schizophrenia groups. Negative voltage is plotted upwards. Waveforms (shown at Cz and Pz) evoked by target pictures that were preceded by prime words that were related to the target's name along three dimensions are shown as solid lines: Semantic (blue), Phonemic (black) and Identity (red). For each of these three relationship types, waveforms produced by the same targets when preceded by unrelated primes are shown as dotted lines. Voltage maps show differences between ERPs evoked by each of these contrasts in the late N400 time window (450–550 ms). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 5

Diagrammatic depiction of proposed processing and adaptation/learning mechanisms engaged when (A) healthy control participants and (B) people with schizophrenia name target pictures that are immediately preceded by masked semantically related prime words. Dotted lines are used to indicate connections across semantic and lexical form levels of representation, with the thickness of the lines depicting the strength of connections. Arrows are used to indicate the flow of activity prior to production. 1. The connections established between the lexical form of the masked prime and its semantic features (dotted lines) are weaker and more diffuse in people with schizophrenia than in healthy control participants. 2. As participants prepare to name the target picture, they retrieve its semantic features and map them on to the target's lexical representation. In both control and patient groups, a subset of these semantic features have been pre-activated by the semantically related prime (dark gray), and so this mapping process is facilitated. Thus, the amplitude of the N400 evoked by semantically related (versus unrelated) targets is reduced in both the control and patient groups. 3. Learning/adaptation is initiated when the selection of the target's lexical form is complete. This entails strengthening the connections between the target's lexical form and its semantic features (indicated using dark dotted lines) and diminishing the strength of any competing connections between the subset of semantic features shared by the prime, and the prime's lexical form (indicated with light dotted lines and crosses). In both control and patient groups, this competitive learning process leads to longer naming times to semantically related than unrelated targets: the behavioral semantic interference effect.

Fig. 6

Diagrammatic depiction of processing and learning mechanisms engaged when (A) healthy control participants and (B) people with schizophrenia name target pictures that are immediately preceded by masked identity related prime words. Dotted lines are used to indicate connections across levels of representation, with the thickness of the lines depicting the strength of connections. Arrows are used to indicate the flow of activity prior to production. 1. The connections established between the lexical form of the masked prime and its semantic features (dotted lines) are weaker and more diffuse in people with schizophrenia than in healthy control participants. 2. As participants prepare to name the target picture, they retrieve its semantic features and map them on to the target's lexical form. Learning/adaptation is initiated when selection of the target's lexical form is complete (this occurs earlier than for semantically related targets because the target's lexical form was pre-activated by the identity related prime). In control participants, this whole process is facilitated in comparison with preparing to name unrelated targets, leading to a smaller N400 amplitude to identity related than unrelated targets. In people with schizophrenia, however, learning/adaptation entails strengthening the connections between the target's lexical form and its semantic features (indicated using dark dotted lines) and diminishing the strength of any competing connections (indicated with light dotted lines and crosses). This competitive learning process leads to a larger N400 amplitude to identity related than to unrelated targets: a reversed N400 effect.