Stress is widely considered to negatively impact hippocampal function, thus impairing episodic memory. However, the hippocampus is not merely the seat of episodic memory. Rather, it also (via distinct circuitry) supports statistical learning. On the basis of rodent work suggesting that stress may impair the hippocampal pathway involved in episodic memory while sparing or enhancing the pathway involved in statistical learning, we developed a behavioral experiment to investigate the effects of acute stress on both episodic memory and statistical learning in humans. Participants were randomly assigned to one of three conditions: stress (socially evaluated cold pressor) immediately before learning, stress ∼15 min before learning, or no stress. In the learning task, participants viewed a series of trial-unique scenes (allowing for episodic encoding of each image) in which certain scene categories reliably followed one another (allowing for statistical learning of associations between paired categories). Memory was assessed 24 hr later to isolate stress effects on encoding/learning rather than retrieval. We found modest support for our hypothesis that acute stress can amplify statistical learning: Only participants stressed ∼15 min in advance exhibited reliable evidence of learning across multiple measures. Furthermore, stress-induced cortisol levels predicted statistical learning retention 24 hr later. In contrast, episodic memory did not differ by stress condition, although we did find preliminary evidence that acute stress promoted memory for statistically predictable information and attenuated competition between statistical and episodic encoding. Together, these findings provide initial insights into how stress may differentially modulate learning processes within the hippocampus.

We encounter the same people, places, and objects in predictable sequences and configurations. Humans efficiently learn these regularities via statistical learning. Importantly, statistical learning creates knowledge not only of specific regularities but also of regularities that apply more generally across related experiences (i.e., across members of a category). Prior evidence for different levels of learning comes from post-exposure behavioral tests, leaving open the question of whether more abstract regularities are detected online during initial exposure. We address this question by measuring neural entrainment in intracranial recordings. Neurosurgical patients viewed a stream of photographs with regularities at one of two levels: In the exemplar-level structured condition, the same photographs appeared repeatedly in pairs. In the category-level structured condition, the photographs were trial-unique but their categories were paired across repetitions. In a baseline random condition, the same photographs repeated but in a scrambled order. We measured entrainment at the frequency of individual photographs, which was expected in all conditions, but critically also at half that frequency—the rate at which to-be-learned pairs appeared in the two structured (but not random) conditions. Entrainment to both exemplar and category pairs emerged within minutes throughout visual cortex and in frontal and temporal regions. Many electrode contacts were sensitive to only one level of structure, but a significant number encoded both levels. These findings suggest that the brain spontaneously uncovers category-level regularities during statistical learning, providing insight into the brain's unsupervised mechanisms for building flexible and robust knowledge that generalizes across input variation and conceptual hierarchies.

Classic taxonomies of memory distinguish explicit and implicit memory systems, placing motor skills squarely in the latter branch. This assertion is in part a consequence of foundational discoveries showing significant motor learning in amnesics. Those findings suggest that declarative memory processes in the medial temporal lobe (MTL) do not contribute to motor learning. Here, we revisit this issue, testing an individual (L. S. J.) with severe MTL damage on four motor learning tasks and comparing her performance to age-matched controls. Consistent with previous findings in amnesics, we observed that L. S. J. could improve motor performance despite having significantly impaired declarative memory. However, she tended to perform poorly relative to age-matched controls, with deficits apparently related to flexible action selection. Further supporting an action selection deficit, L. S. J. fully failed to learn a task that required the acquisition of arbitrary action–outcome associations. We thus propose a modest revision to the classic taxonomic model: Although MTL-dependent memory processes are not necessary for some motor learning to occur, they play a significant role in the acquisition, implementation, and retrieval of action selection strategies. These findings have implications for our understanding of the neural correlates of motor learning, the psychological mechanisms of skill, and the theory of multiple memory systems.

Humans perceive expected stimuli faster and more accurately. However, the mechanism behind the integration of expectations with sensory information during perception remains unclear. We investigated the hypothesis that such integration depends on “fusion”—the weighted averaging of different cues informative about stimulus identity. We first trained participants to map a range of tones onto faces spanning a male–female continuum via associative learning. These two features served as expectation and sensory cues to sex, respectively. We then tested specific predictions about the consequences of fusion by manipulating the congruence of these cues in psychophysical and fMRI experiments. Behavioral judgments and patterns of neural activity in auditory association regions revealed fusion of sensory and expectation cues, providing evidence for a precise computational account of how expectations influence perception.

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.

Top–down attention prioritizes the processing of goal-relevant information throughout visual cortex based on where that information is found in space and what it looks like. Whereas attentional goals often have both spatial and featural components, most research on the neural basis of attention has examined these components separately. Here we investigated how these attentional components are integrated by examining the attentional modulation of functional connectivity between visual areas with different selectivity. Specifically, we used fMRI to measure temporal correlations between spatially selective regions of early visual cortex and category-selective regions in ventral temporal cortex while participants performed a task that benefitted from both spatial and categorical attention. We found that categorical attention modulated the connectivity of category-selective areas, but only with retinotopic areas that coded for the spatially attended location. Similarly, spatial attention modulated the connectivity of retinotopic areas only with the areas coding for the attended category. This pattern of results suggests that attentional modulation of connectivity is driven both by spatial selection and featural biases. Combined with exploratory analyses of frontoparietal areas that track these changes in connectivity among visual areas, this study begins to shed light on how different components of attention are integrated in support of more complex behavioral goals.

The posterior medial network is at the apex of a temporal integration hierarchy in the brain, integrating information over many seconds of viewing intact, but not scrambled, movies. This has been interpreted as an effect of temporal structure. Such structure in movies depends on preexisting event schemas, but temporal structure can also arise de novo from learning. Here, we examined the relative role of schema-consistent temporal structure and arbitrary but consistent temporal structure on the human posterior medial network. We tested whether, with repeated viewing, the network becomes engaged by scrambled movies with temporal structure. Replicating prior studies, activity in posterior medial regions was immediately locked to stimulus structure upon exposure to intact, but not scrambled, movies. However, for temporally structured scrambled movies, functional coupling within the network increased across stimulus repetitions, rising to the level of intact movies. Thus, temporal structure is a key determinant of network dynamics and function in the posterior medial network.

Despite the importance of learning and remembering across the lifespan, little is known about how the episodic memory system develops to support the extraction of associative structure from the environment. Here, we relate individual differences in volumes along the hippocampal long axis to performance on statistical learning and associative inference tasks—both of which require encoding associations that span multiple episodes—in a developmental sample ranging from ages 6 to 30 years. Relating age to volume, we found dissociable patterns across the hippocampal long axis, with opposite nonlinear volume changes in the head and body. These structural differences were paralleled by performance gains across the age range on both tasks, suggesting improvements in the cross-episode binding ability from childhood to adulthood. Controlling for age, we also found that smaller hippocampal heads were associated with superior behavioral performance on both tasks, consistent with this region's hypothesized role in forming generalized codes spanning events. Collectively, these results highlight the importance of examining hippocampal development as a function of position along the hippocampal axis and suggest that the hippocampal head is particularly important in encoding associative structure across development.

A key task for the brain is to determine which pieces of information are worth storing in memory. To build a more complete representation of the environment, memory systems may prioritize new information that has not already been stored. Here, we propose a mechanism that supports this preferential encoding of new information, whereby prior experience attenuates neural activity for old information that is competing for processing. We evaluated this hypothesis with fMRI by presenting a series of novel stimuli concurrently with repeated stimuli at different spatial locations in Experiment 1 and from different visual categories (i.e., faces and scenes) in Experiment 2. Subsequent memory for the novel stimuli could be predicted from the reduction in activity in ventral temporal cortex for the accompanying repeated stimuli. This relationship was eliminated in control conditions where the competition during encoding came from another novel stimulus. These findings reveal how prior experience adaptively guides learning toward new aspects of the environment.

The sensory input that we experience is highly patterned, and we are experts at detecting these regularities. Although the extraction of such regularities, or statistical learning (SL), is typically viewed as a cortical process, recent studies have implicated the medial temporal lobe (MTL), including the hippocampus. These studies have employed fMRI, leaving open the possibility that the MTL is involved but not necessary for SL. Here, we examined this issue in a case study of LSJ, a patient with complete bilateral hippocampal loss and broader MTL damage. In Experiments 1 and 2, LSJ and matched control participants were passively exposed to a continuous sequence of shapes, syllables, scenes, or tones containing temporal regularities in the co-occurrence of items. In a subsequent test phase, the control groups exhibited reliable SL in all conditions, successfully discriminating regularities from recombinations of the same items into novel foil sequences. LSJ, however, exhibited no SL, failing to discriminate regularities from foils. Experiment 3 ruled out more general explanations for this failure, such as inattention during exposure or difficulty following test instructions, by showing that LSJ could discriminate which individual items had been exposed. These findings provide converging support for the importance of the MTL in extracting temporal regularities.

There is a well-established posterior network of cortical regions that plays a central role in face processing and that has been investigated extensively. In contrast, although responsive to faces, the amygdala is not considered a core face-selective region, and its face selectivity has never been a topic of systematic research in human neuroimaging studies. Here, we conducted a large-scale group analysis of fMRI data from 215 participants. We replicated the posterior network observed in prior studies but found equally robust and reliable responses to faces in the amygdala. These responses were detectable in most individual participants, but they were also highly sensitive to the initial statistical threshold and habituated more rapidly than the responses in posterior face-selective regions. A multivariate analysis showed that the pattern of responses to faces across voxels in the amygdala had high reliability over time. Finally, functional connectivity analyses showed stronger coupling between the amygdala and posterior face-selective regions during the perception of faces than during the perception of control visual categories. These findings suggest that the amygdala should be considered a core face-selective region.

A quintessential example of hemispheric specialization in the human brain is that the right hemisphere is specialized for face perception. However, because the visual system is organized contralaterally, what happens when faces appear in the right visual field and are projected to the nonspecialized left hemisphere? We used divided field presentation and fMRI adaptation to test the hypothesis that the left hemisphere can recognize faces, but only with support from the right hemisphere. Consistent with this hypothesis, facial identity adaptation was observed in the left fusiform face area when a face had previously been processed by the right hemisphere, but not when it had only been processed by the left hemisphere. These results imply that facial identity information is transferred from the right hemisphere to the left hemisphere, and that the left hemisphere can represent facial identity but is less efficient at extracting this information by itself.

Our environment contains regularities distributed in space and time that can be detected by way of statistical learning. This unsupervised learning occurs without intent or awareness, but little is known about how it relates to other types of learning, how it affects perceptual processing, and how quickly it can occur. Here we use fMRI during statistical learning to explore these questions. Participants viewed statistically structured versus unstructured sequences of shapes while performing a task unrelated to the structure. Robust neural responses to statistical structure were observed, and these responses were notable in four ways: First, responses to structure were observed in the striatum and medial temporal lobe, suggesting that statistical learning may be related to other forms of associative learning and relational memory. Second, statistical regularities yielded greater activation in category-specific visual regions (object-selective lateral occipital cortex and word-selective ventral occipito-temporal cortex), demonstrating that these regions are sensitive to information distributed in time. Third, evidence of learning emerged early during familiarization, showing that statistical learning can operate very quickly and with little exposure. Finally, neural signatures of learning were dissociable from subsequent explicit familiarity, suggesting that learning can occur in the absence of awareness. Overall, our findings help elucidate the underlying nature of statistical learning.

Cognition constantly involves retrieving and maintaining information that is not perceptually available in the current environment. Studies on visual imagery and working memory suggest that such high-level cognition might, in part, be mediated by the revival of perceptual representations in the inferior temporal cortex. Here, we provide new support for this hypothesis, showing that reflectively accessed information can have similar consequences for subsequent perception as actual perceptual input. Participants were presented with pairs of frames in which a scene could appear, and were required to make a category judgment on the second frame. In the critical condition, a scene was presented in the first frame, but the second frame was blank. Thus, it was necessary to refresh the scene from the first frame in order to make the category judgment. Scenes were then repeated in subsequent trials to measure the effect of refreshing on functional magnetic resonance imaging repetition attenuation—a neural index of memory—in a scene-selective region of the visual cortex. Surprisingly, the refreshed scenes produced equal attenuation as scenes that had been presented twice during encoding, and more attenuation than scenes that had been presented once during encoding, but that were not refreshed. Thus, the top-down revival of a percept had a similar effect on memory as actually seeing the stimulus again. These findings indicate that high-level cognition can activate stimulus-specific representations in the ventral visual cortex, and that such top-down activation, like that from sensory stimulation, produces memorial changes that affect perceptual processing during a later encounter with the stimulus.