Content-based Dissociation of Hippocampal Involvement in Prediction

Recent work suggests that a key function of the hippocampus is to predict the future. This is thought to depend on its ability to bind inputs over time and space and to retrieve upcoming or missing inputs based on partial cues. In line with this, previous research has revealed prediction-related signals in the hippocampus for complex visual objects, such as fractals and abstract shapes. Implicit in such accounts is that these computations in the hippocampus reflect domain-general processes that apply across different types and modalities of stimuli. An alternative is that the hippocampus plays a more domain-specific role in predictive processing, with the type of stimuli being predicted determining its involvement. To investigate this, we compared hippocampal responses to auditory cues predicting abstract shapes (Experiment 1) versus oriented gratings (Experiment 2). We measured brain activity in male and female human participants using high-resolution fMRI, in combination with inverted encoding models to reconstruct shape and orientation information. Our results revealed that expectations about shape and orientation evoked distinct representations in the hippocampus. For complex shapes, the hippocampus represented which shape was expected, potentially serving as a source of top-down predictions. In contrast, for simple gratings, the hippocampus represented only unexpected orientations, more reminiscent of a prediction error. We discuss several potential explanations for this content-based dissociation in hippocampal function, concluding that the computational role of the hippocampus in predictive processing may depend on the nature and complexity of stimuli

Face-Specific Resting Functional Connectivity between the Fusiform Gyrus and Posterior Superior Temporal Sulcus

Faces activate specific brain regions in fMRI, including the fusiform gyrus (FG) and the posterior superior temporal sulcus (pSTS). The fact that the FG and pSTS are frequently co-activated suggests that they may interact synergistically in a distributed face processing network. Alternatively, the functions implemented by these regions may be encapsulated from each other. It has proven difficult to evaluate these two accounts during visual processing of face stimuli. However, if the FG and pSTS interact during face processing, the substrate for such interactions may be apparent in a correlation of the BOLD timeseries from these two regions during periods of rest when no faces are present. To examine face-specific resting correlations, we developed a new partial functional connectivity approach in which we removed variance from the FG that was shared with other category-selective and control regions. The remaining face-specific FG resting variance was then used to predict resting signals throughout the brain. In two experiments, we observed face-specific resting functional connectivity between FG and pSTS, and importantly, these correlations overlapped precisely with the face-specific pSTS region obtained from independent localizer runs. Additional region-of-interest and pattern analyses confirmed that the FG–pSTS resting correlations were face-specific. These findings support a model in which face processing is distributed among a finite number of connected, but nevertheless face-specialized regions. The discovery of category-specific interactions in the absence of visual input suggests that resting networks may provide a latent foundation for task processing

Babies and Brains: Habituation in Infant Cognition and Functional Neuroimaging

Many prominent studies of infant cognition over the past two decades have relied on the fact that infants habituate to repeated stimuli – i.e. that their looking times tend to decline upon repeated stimulus presentations. This phenomenon had been exploited to reveal a great deal about the minds of preverbal infants. Many prominent studies of the neural bases of adult cognition over the past decade have relied on the fact that brain regions habituate to repeated stimuli – i.e. that the hemodynamic responses observed in fMRI tend to decline upon repeated stimulus presentations. This phenomenon has been exploited to reveal a great deal about the neural mechanisms of perception and cognition. Similarities in the mechanics of these two forms of habituation suggest that it may be useful to relate them to each other. Here we outline this analogy, explore its nuances, and highlight some ways in which the study of habituation in functional neuroimaging could yield novel insights into the nature of habituation in infant cognition – and vice versa

Associative Prediction of Visual Shape in the Hippocampus

Perception can be cast as a process of inference, in which bottom-up signals are combined with top-down predictions in sensory systems. In line with this, neural activity in sensory cortex is strongly modulated by prior expectations. Such top-down predictions often arise from cross-modal associations, such as when a sound (e.g., bell or bark) leads to an expectation of the visual appearance of the corresponding object (e.g., bicycle or dog). We hypothesized that the hippocampus, which rapidly learns arbitrary relationships between stimuli over space and time, may be involved in forming such associative predictions. We exposed male and female human participants to auditory cues predicting visual shapes, while measuring high-resolution fMRI signals in visual cortex and the hippocampus. Using multivariate reconstruction methods, we discovered a dissociation between these regions: representations in visual cortex were dominated by whichever shape was presented, whereas representations in the hippocampus reflected only which shape was predicted by the cue. The strength of hippocampal predictions correlated across participants with the amount of expectation-related facilitation in visual cortex. These findings help bridge the gap between memory and sensory systems in the human brain

Across space and time: infants learn from backward and forward visual statistics

within temporal and spatial visual streams. Two groups of 8-month-old infants were familiarized with an artificial grammar of shapes, comprised of backward and forward base pairs (i.e., two shapes linked by strong backward or forward transitional probability) and part-pairs (i.e., two shapes with weak transitional probabilities in both directions). One group viewed the continuous visual stream as a temporal sequence, while the other group viewed the same stream as a spatial array. Following familiarization, infants looked longer at test trials containing part- pairs than base pairs, though they had appeared with equal frequency during familiarization. This pattern of looking time was evident for both forward and backward pairs, in both the temporal and spatial conditions. Further, differences in looking time to part-pairs that were consistent or inconsistent with the predictive direction of the base pairs (forward or backward) indicated that infants were indeed sensitive to direction when presented with temporal sequences, but not when presented with spatial arrays. These results suggest that visual statistical learning is flexible in infancy and depends on the nature of visual input

Learning hierarchical sequence representations across human cortex and hippocampus

Sensory input arrives in continuous sequences that humans experience as segmented units, e.g., words and events. The brain’s ability to discover regularities is called statistical learning. Structure can be represented at multiple levels, including transitional probabilities, ordinal position, and identity of units. To investigate sequence encoding in cortex and hippocampus, we recorded from intracranial electrodes in human subjects as they were exposed to auditory and visual sequences containing temporal regularities. We find neural tracking of regularities within minutes, with characteristic profiles across brain areas. Early processing tracked lower-level features (e.g., syllables) and learned units (e.g., words), while later processing tracked only learned units. Learning rapidly shaped neural representations, with a gradient of complexity from early brain areas encoding transitional probability, to associative regions and hippocampus encoding ordinal position and identity of units. These findings indicate the existence of multiple, parallel computational systems for sequence learning across hierarchically organized cortico-hippocampal circuits

Neurocognitive therapeutics: from concept to application in the treatment of negative attention bias

There is growing interest in the use of neuroimaging for the direct treatment of mental illness. Here, we present a new framework for such treatment, neurocognitive therapeutics. What distinguishes neurocognitive therapeutics from prior approaches is the use of precise brain-decoding techniques within a real-time feedback system, in order to adapt treatment online and tailor feedback to individuals’ needs. We report an initial feasibility study that uses this framework to alter negative attention bias in a small number of patients experiencing significant mood symptoms. The results are consistent with the promise of neurocognitive therapeutics to improve mood symptoms and alter brain networks mediating attentional control. Future work should focus on optimizing the approach, validating its effectiveness, and expanding the scope of targeted disorders

Cross-Modal Transfer of Statistical Information Benefits from Sleep

Extracting regularities from a sequence of events is essential for understanding our environment. However, there is no consensus regarding the extent to which such regularities can be generalised beyond the modality of learning. One reason for this could be the variation in consolidation intervals used in different paradigms, also including an opportunity to sleep. Using a novel statistical learning paradigm in which structured information is acquired in the auditory domain and tested in the visual domain over either 30min or 24hr consolidation intervals, we show that cross-modal transfer can occur, but this transfer is only seen in the 24hr group. Importantly, the extent of cross-modal transfer is predicted by the amount of SWS obtained. Additionally, cross-modal transfer is associated with the same pattern of decreasing MTL and increasing striatal involvement which has previously been observed to occur across 24 hours in unimodal statistical learning. We also observed enhanced functional connectivity after 24 hours in a network of areas which have been implicated in cross-modal integration including the precuneus and the middle occipital gyrus. Finally, functional connectivity between the striatum and the precuneus was also enhanced, and this strengthening was predicted by SWS. These results demonstrate that statistical learning can generalise to some extent beyond the modality of acquisition, and together with our previously published unimodal results, support the notion that statistical learning is both domain-general and domain-specific