How silent is silent reading? Intracerebral evidence for top-down activation of temporal voice areas during reading

Abstract

As you might experience it while reading this sentence, silent reading often involves an imagery speech component: we can hear our own "inner voice" pronouncing words mentally. Recent functional magnetic resonance imaging studies have associated that component with increased metabolic activity in the auditory cortex, including voice-selective areas. It remains to be determined, however, whether this activation arises automatically from early bottom-up visual inputs or whether it depends on late top-down control processes modulated by task demands. To answer this question, we collaborated with four epileptic human patients recorded with intracranial electrodes in the auditory cortex for therapeutic purposes, and measured high-frequency (50-150 Hz) "gamma" activity as a proxy of population level spiking activity. Temporal voice-selective areas (TVAs) were identified with an auditory localizer task and monitored as participants viewed words flashed on screen. We compared neural responses depending on whether words were attended or ignored and found a significant increase of neural activity in response to words, strongly enhanced by attention. In one of the patients, we could record that response at 800 ms in TVAs, but also at 700 ms in the primary auditory cortex and at 300 ms in the ventral occipital temporal cortex. Furthermore, single-trial analysis revealed a considerable jitter between activation peaks in visual and auditory cortices. Altogether, our results demonstrate that the multimodal mental experience of reading is in fact a heterogeneous complex of asynchronous neural responses, and that auditory and visual modalities often process distinct temporal frames of our environment at the same time.

Figures

Figure 1.

Anatomical location of recording sites. Black crosshairs indicate site location on coronal and axial views of individual MRI.

Figure 2.

Selectivity to speech in the auditory cortex. Bar plots show the mean HFA (±SEM) measured while participants listened to sounds of several categories (averaged across 60 nonoverlapping 500 ms windows during sounds, see Materials and Methods). HFA is expressed in percentage of the average amplitude measured across the entire recording session. Values with a colored asterisk are significant higher than values indicated by a bracket of the same color (Kruskal–Wallis, post hoc pairwise comparison). Note that in P2 and P4 the French sentence did not elicit a response significantly stronger than to animal sounds, but the sites were nevertheless included in the study because of the strong response to other speech-like stimuli (Revers and Suomi).

Figure 3.

Correspondence between recording sites and TVAs. For each site, blue crosshairs indicate its normalized MNI coordinates projected upon the single-subject MRI. Red overlay shows the probabilistic map of TVA, as defined by Belin et al. (2000). (TVA map available for download at http://vnl.psy.gla.ac.uk/resources.php.)

Figure 4.

Response to written words in TVAs. For each site, plots display HFA modulations (50–150 Hz) averaged across trials in the two attention conditions (±SEM): Attend (blue) and Ignore (red). Amplitude is expressed in percentage of the average amplitude measured across the entire recording session. Shaded areas indicate time windows during which HFA is significantly higher in the Attend condition. Words were presented at 0 ms for 100 ms. Note that in that dataset, the probability for the preceding word to be attended or ignored is the same (50%).

Figure 5.

Response to sounds in the primary auditory cortex. Bar plots show the mean HFA (±SEM) measured while participants listened to sounds of several categories (averaged across 60 nonoverlapping 500 ms windows during sounds, see Materials and Methods). Values with a colored asterisk are significant higher than values indicated by a bracket of the same color (Kruskal–Wallis, post hoc pairwise comparison). HFA is expressed in percentage of the average amplitude measured across the entire recording session. Note that speech-like and nonspeech-like sounds elicit equally strong responses.

Figure 6.

Neural response to written words in the visual and auditory cortex. The three sites were recorded in the same patient, P2, in the left VOTC (F′2), the primary auditory cortex (U2), and in a TVA, in the STG (T7), respectively. Plots display HFA modulations (50–150 Hz) averaged across trials in the two attention conditions (±SEM): Attend (blue) and Ignore (red), for each site. Amplitude is expressed in percentage of the average amplitude measured across the entire recording session. Words were presented at 0 ms for 100 ms. Note that in that dataset, the probability for the preceding word to be attended (Attend) or ignored (Ignore) is the same (50%). However, the upcoming word shown at 700 ms has a higher probability to be of the opposite condition. This explains the second peak of activation ∼1000 ms in T7 (red curve).

Figure 7.

Single-trial responses to written words in visual and auditory cortex. Plots are HFA fluctuations (50–150 Hz) during the reading task. Vertical lines indicate word onsets in the Attend (blue) and Ignore (red) conditions. Individual activation peaks can be seen in VOTC (F′2) and the primary auditory cortex (U2). Note that the lag between visual and auditory peaks is not constant.

Figure 8.

Directed interactions between VOTC and the primary auditory cortex. Difference between the Granger Causality terms quantifying the directed interactions from VOTC to primary auditory cortex and vice versa for the Attend (black) and Ignore (gray) condition; positive values indicate more influence from VOTC to primary auditory cortex. Time windows showing significant (p < 0.01) differences of influence are marked by shaded area. Time windows showing significant (p < 0.01) differences of influence are shaded in gray (indicating significance in the Attend condition).