The effect of context congruency on fMRI repetition suppression for objects.

The recognition of objects is strongly facilitated when they are presented in the context of other objects (Biederman, 1972). Such contexts facilitate perception and induce expectations of context-congruent objects (Trapp and Bar, 2015). The neural mechanisms underlying these facilitatory effects of context on object processing, however, are not yet fully understood. In the present study, we investigate how context-induced expectations affect subsequent object processing. We used functional magnetic resonance imaging and measured repetition suppression as a proxy for prediction error processing. Participants viewed pairs of alternating or repeated object images which were preceded by context-congruent, context-incongruent or neutral cues. We found a stronger repetition suppression in congruent as compared to incongruent or neutral cues in the object sensitive lateral occipital cortex. Interestingly, this stronger effect was driven by enhanced responses to alternating stimulus pairs in the congruent contexts, rather than by suppressed responses to repeated stimulus pairs, which emphasizes the contribution of surprise-related response enhancement for the context modulation on RS when expectations are violated. In addition, in the congruent condition, we discovered significant functional connectivity between object-responsive and frontal cortical regions, as well as between object-responsive regions and the fusiform gyrus. Our findings indicate that prediction errors, reflected in enhanced brain responses to violated contextual expectations, underlie the facilitating effect of context during object perception.

Person identity-specific adaptation effects in the ventral occipito-temporal cortex.

Identifying the faces of familiar persons requires the ability to assign several different images of a face to a common identity. Previous research showed that the occipito-temporal cortex, including the fusiform and the occipital face areas, is sensitive to personal identity. Still, the viewpoint, facial expression and image-independence of this information are currently under heavy debate. Here we adapted a rapid serial visual stimulation paradigm Johnston et al. (2016, https://doi.org/10.1016/j.cortex.2016.10.002) and presented highly variable ambient-face images of famous persons to measure functional magnetic resonance imaging (fMRI) adaptation. fMRI adaptation is considered as the neuroimaging manifestation of repetition suppression, a neural phenomenon currently explained as a correlate of reduced predictive error responses for expected stimuli. We revisited the question of image-invariant identity-specific encoding mechanisms of the occipito-temporal cortex, using fMRI adaptation with a particular interest in predictive mechanisms. Participants were presented with trials containing eight different images of a famous person, images of eight different famous persons or seven different images of a particular famous person followed by an identity change to violate potential expectation effects about person identity. We found an image-independent adaptation effect of identity for famous faces in the fusiform face area. However, in contrast to previous electrophysiological studies, using similar paradigms, no release of the adaptation effect was observed when identity-specific expectations were violated. Our results support recent multivariate pattern analysis studies, showing image-independent identity encoding in the core face-processing areas of the occipito-temporal cortex. These results are discussed in the frame of recent identity-processing models and predictive mechanisms.

Measures of repetition suppression in the fusiform face area are inflated by co-occurring effects of statistically learned visual associations.

Repeated presentation of a stimulus leads to reductions in measures of neural responses. This phenomenon, termed repetition suppression (RS), has recently been conceptualized using models based on predictive coding, which describe RS as due to expectations that are weighted toward recently-seen stimuli. To evaluate these models, researchers have manipulated the likelihood of stimulus repetition within experiments. They have reported findings that are inconsistent across hemodynamic and electrophysiological measures, and difficult to interpret as clear support or refutation of predictive coding models. We instead investigated a different type of expectation effect that is apparent in stimulus repetition experiments: the difference in one's ability to predict the identity of repeated, compared to unrepeated, stimuli. In previous experiments that presented pairs of repeated or alternating images, once participants had seen the first stimulus image in a pair, they could form specific expectations about the repeated stimulus image but not the alternating image, which was often randomly chosen from a large stimulus set. To assess the contribution of stimulus predictability effects to previously observed RS, we measured BOLD signals while presenting pairs of repeated and alternating faces. This was done in contexts whereby stimuli in alternating trials were either i.) predictable through statistically learned associations between pairs of stimuli or ii.) chosen randomly and therefore unpredictable. We found that RS in the right fusiform face area (FFA) was much larger in trials with unpredictable compared to predictable alternating faces. This was primarily due to unpredictable alternating stimuli evoking larger BOLD signals than predictable alternating stimuli. We show that imbalances in stimulus predictability across repeated and alternating trials can greatly inflate measures of RS, and potentially even mimic RS effects. Our findings indicate that stimulus-specific expectations as described by predictive coding models may account for a sizeable portion of observed RS effects.

The occipital face area is causally involved in identity-related visual-semantic associations.

Faces are processed in a network of areas within regions of the ventral visual stream. However, familiar faces typically are characterized by additional associated information, such as episodic memories or semantic biographical information as well. The acquisition of such non-sensory, identity-specific knowledge plays a crucial role in our ability to recognize and identify someone we know. The occipital face area (OFA), an early part of the core face-processing network, is recently found to be involved in the formation of identity-specific memory traces but it is currently unclear if this role is limited to unimodal visual information. The current experiments used transcranial magnetic stimulation (TMS) to test whether the OFA is involved in the association of a face with identity-specific semantic information, such as the name or job title of a person. We applied an identity-learning task where unfamiliar faces were presented together with a name and a job title in the first encoding phase. Simultaneously, TMS pulses were applied either to the left or right OFA or to Cz, as a control. In the subsequent retrieval phase, the previously seen faces were presented either with two names or with two job titles and the task of the participants was to select the semantic information previously learned. We found that the stimulation of the right or left OFA reduced subsequent retrieval performance for the face-associated job titles. This suggests a causal role of the OFA in the association of faces and related semantic information. Furthermore, in contrast to prior findings, we did not observe hemispherical differences of the TMS intervention, suggesting a similar role of the left and right OFAs in the formation of the visual-semantic associations. Our results suggest the necessity to reconsider the hierarchical face-perception models and support the distributed and recurrent models.

Repetition Suppression for Noisy and Intact Faces in the Occipito-Temporal Cortex.

Repetition suppression (RS), the relative lower neural response magnitude to repeated as compared to non-repeated stimuli, is often explained within the predictive coding framework. According to this theory, precise predictions (priors) together with less precise sensory evidences lead to decisions that are determined largely by the predictions and the other way around. In other words, the prediction error, namely the magnitude of RS, should depend on the precision of predictions and sensory inputs. In the current study, we aimed at testing this idea by manipulating the clarity and thereby the precision of the incoming sensory data by adding noise to the images. This resulted in an fMRI adaptation design with repeated or alternating trials showing clear or noisy face stimuli. Our results show a noise effect on the activity in the fusiform face area (FFA), namely less activation for noisy than for clear trials, which supports previous findings. No such effects could be found in OFA or LO. Data also showed reliable RS in the FFA (bilateral) and unilaterally in OFA (right) and LO (left). Interestingly, the noise added to the stimuli did not affect the magnitude of RS in any of the tested cortical areas. This suggests that the clarity of the sensory input is not crucial in determining the magnitude of RS.

Similar Expectation Effects for Immediate and Delayed Stimulus Repetitions.

A prior cue or stimulus allows prediction of the future occurrence of an event and therefore reduces the associated neural activity in several cortical areas. This phenomenon is labeled expectation suppression (ES) and has recently been shown to be independent of the generally observed effects of stimulus repetitions (repetition suppression, RS: reduced neuronal response after the repetition of a given stimulus). While it has been shown that attentional cueing is strongly affected by the length of the cue-target delay, we have no information on the temporal dynamics of expectation effects, as in most prior studies of ES the delay between the predictive cue and the target (i.e., the inter-stimulus interval, ISI) was in the range of a few hundred milliseconds. Hence, we presented participants with pairs of faces where the first face could be used to build expectations regarding the second one, in the sense that one gender indicated repetition of the same face while the other gender predicted the occurrence of novel faces. In addition, we presented the stimulus pairs with two different ISIs (0.5 s for Immediate and 1.75 or 3.75 s for Delayed ISIs). We found significant RS as well as a reduced response for correctly predicted when compared to surprising trials in the fusiform face area. Importantly, the effects of repetition and expectation were both independent of the length of the ISI period. This implies that Immediate and Delayed cue-target stimulus arrangements lead to similar expectation effects in the face sensitive-visual cortex.