When making a turn at a familiar intersection, we know what items and landmarks will come into view. These perceptual expectations, or predictions, come from our knowledge of the context; however, it is unclear how memory and perceptual systems interact to support the prediction and reactivation of sensory details in cortex. To address this, human participants learned the spatial layout of animals positioned in a cross maze. During fMRI, participants of both sexes navigated between animals to reach a target, and in the process saw a predictable sequence of five animal images. Critically, to isolate activity patterns related to item predictions, rather than bottom-up inputs, one-fourth of trials ended early, with a blank screen presented instead. Using multivariate pattern similarity analysis, we reveal that activity patterns in early visual cortex, posterior medial regions, and the posterior hippocampus showed greater similarity when seeing the same item compared with different items. Further, item effects in posterior hippocampus were specific to the sequence context. Critically, activity patterns associated with seeing an item in visual cortex and posterior medial cortex, were also related to activity patterns when an item was expected, but omitted, suggesting sequence predictions were reinstated in these regions. Finally, multivariate connectivity showed that patterns in the posterior hippocampus at one position in the sequence were related to patterns in early visual cortex and posterior medial cortex at a later position. Together, our results support the idea that hippocampal representations facilitate sensory processing by modulating visual cortical activity in anticipation of expected items.SIGNIFICANCE STATEMENT Our visual world is a series of connected events, where we can predict what we might see next based on our recent past. Understanding the neural circuitry and mechanisms of the perceptual and memory systems that support these expectations is fundamental to revealing how we perceive and act in our world. Using brain imaging, we studied what happens when we expect to see specific visual items, and how such expectations relate to top-down memory signals. We find both visual and memory systems reflect item predictions, and moreover, we show that hippocampal activity supports predictions of future expected items. This demonstrates that the hippocampus acts to predict upcoming items, and reinstates such predictions in cortex.

Recent work in cognitive and systems neuroscience has suggested that the hippocampus might support planning, imagination, and navigation by forming cognitive maps that capture the abstract structure of physical spaces, tasks, and situations. Navigation involves disambiguating similar contexts, and the planning and execution of a sequence of decisions to reach a goal. Here, we examine hippocampal activity patterns in humans during a goal-directed navigation task to investigate how contextual and goal information are incorporated in the construction and execution of navigational plans. During planning, hippocampal pattern similarity is enhanced across routes that share a context and a goal. During navigation, we observe prospective activation in the hippocampus that reflects the retrieval of pattern information related to a key-decision point. These results suggest that, rather than simply representing overlapping associations or state transitions, hippocampal activity patterns are shaped by context and goals.

Remembering is a complex process that involves recalling specific details, such as who you were with when you celebrated your last birthday, as well as contextual information, such as the place where you celebrated. It is well established that the act of remembering enhances long-term retention of the retrieved information, but the neural and cognitive mechanisms that drive memory enhancement are not yet understood. One possibility is that the process of remembering results in reactivation of the broader episodic context. Consistent with this idea, in two experiments, we found that multiple retrieval attempts enhanced long-term retention of both the retrieved object and the nontarget object that shared scene context, compared with a restudy control. Using representational similarity analysis of fMRI data in experiment 2, we found that retrieval resulted in greater neural reactivation of both the target objects and contextually linked objects compared with restudy. Furthermore, this reactivation occurred in a network of medial and lateral parietal lobe regions that have been linked to episodic recollection. The results demonstrate that retrieving a memory can enhance retention of information that is linked in the broader event context and the hippocampus and a posterior medial network of parietal cortical areas (also known as the Default Network) play complementary roles in supporting the reactivation of episodically linked information during retrieval.

Word retrieval is core to language production and relies on complementary processes: the rapid activation of lexical and conceptual representations and word selection, which chooses the correct word among semantically related competitors. Lexical and conceptual activation is measured by semantic priming. In contrast, word selection is indexed by semantic interference and is hampered in semantically homogeneous (HOM) contexts. We examined the spatiotemporal dynamics of these complementary processes in a picture naming task with blocks of semantically heterogeneous (HET) or HOM stimuli. We used electrocorticography data obtained from frontal and temporal cortices, permitting detailed spatiotemporal analysis of word retrieval processes. A semantic interference effect was observed with naming latencies longer in HOM versus HET blocks. Cortical response strength as indexed by high-frequency band (HFB) activity (70-150 Hz) amplitude revealed effects linked to lexical-semantic activation and word selection observed in widespread regions of the cortical mantle. Depending on the subsecond timing and cortical region, HFB indexed semantic interference (i.e., more activity in HOM than HET blocks) or semantic priming effects (i.e., more activity in HET than HOM blocks). These effects overlapped in time and space in the left posterior inferior temporal gyrus and the left prefrontal cortex. The data do not support a modular view of word retrieval in speech production but rather support substantial overlap of lexical-semantic activation and word selection mechanisms in the brain.