A neural oscillatory signature of reference

The ability to use linguistic representations to refer to the world is a vital mechanism that gives human language its communicative power. In particular, the anaphoric use of words to refer to previously mentioned concepts (antecedents) is what allows dialogue to be coherent and meaningful. Psycholinguistic theory posits that anaphor comprehension involves reactivating an episodic memory representation of the antecedent [1-2]. Whereas this implies the involvement of memory structures, the neural processes for reference resolution are largely unknown. Here, we report time-frequency analysis of four EEG experiments [3-6], revealing the increased coupling of functional neural systems associated with coherent referring expressions compared to referentially ambiguous expressions. We performed time-frequency analysis on data from four experiments in which referentially ambiguous expressions elicited a sustained negativity in the ERP waveform compared to coherent expressions. In Experiment 1, 32 participants read 120 correct Dutch sentences with coherent or ambiguous pronouns. In Experiment 2, 31 participants listened to 90 naturally spoken Dutch mini-stories containing coherent or ambiguous NP anaphora. In Experiment 3, 22 participants each read 60 Spanish sentences with a coherent or ambiguous ellipsis determiner. In Experiment 4, 19 participants each read 180 grammatically correct English sentences containing coherent or ambiguous pronouns. Analysis was performed with Fieldtrip [7], separately for low frequency (2-30 Hz) and high frequency (25-90 Hz) activity. Power-changes per trial were computed as a relative change from a pre-CW baseline interval, average power changes were computed per subject for coherent and ambiguous conditions separately. Statistical tests used cluster-based random permutation [8]. Despite varying in modality, language and type of expression, all experiments showed larger gamma-band power around 80 Hz for coherence compared to ambiguity, within a similar time range. No differences were observed in low frequencies. In high-density EEG Experiment 4, an additional short-duration gamma-increase was observed around 40 Hz, around 300-500 ms after pronoun-onset, which was localised using Beamformer analysis [9] to left posterior parietal cortex (PPC). The 80 Hz power increase around 600-1200 ms after word onset was localised to left inferior frontal-temporal cortex. We argue that the observed gamma-band power increases reflect successful referential binding and resolution, linking incoming information to previously encountered concepts and integrates that information into the unfolding discourse representation. Specifically, we argue that this involves antecedent reactivation in the PPC episodic memory network [10-11], interacting with unification processes in the frontal-temporal language network [12]. Based on these results, and on results of patient [13] and fMRI [14] research on pronoun comprehension, we propose an initial neurobiological account of reference, by bridging the psycholinguistics of anaphora with the neurobiology of language and of episodic memory. [1] Dell et al., 1983 [2] Gerrig & McKoon, 1998 [3] Nieuwland & Van Berkum, 2006 [4] Nieuwland et al., 2007a [5] Martin et al., 2012 [6] Nieuwland, 2014 [7] Oostenveld et al., 2011 [8] Maris & Oostenveld, 2007 [9] Gross et al., 2001 [10] Shannon & Buckner, 2004 [11] Wager et al., 2005 [12] Hagoort & Indefrey, 2014 [13] Kurczek et al., 2013 [14] Nieuwland et al., 2007