Thanks to patients Phineas Gage and Henry Molaison, we have long known that behavioral control depends on the frontal lobes, whereas declarative memory depends on the medial temporal lobes (MTL). For decades, cognitive functions—behavioral control, declarative memory—have served as labels for characterizing the division of labor in cortex. This approach has made enormous contributions to understanding how the brain enables the mind, providing a systems-level explanation of brain function that constrains lower-level investigations of neural mechanism. Today, the approach has evolved such that functional labels are often applied to brain networks rather than focal brain regions. Furthermore, the labels have diversified to include both broadly-defined cognitive functions (declarative memory, visual perception) and more circumscribed mental processes (recollection, familiarity, priming). We ask whether a process—a high-level mental phenomenon corresponding to an introspectively-identifiable cognitive event—is the most productive label for dissecting memory. For example, recollection conflates a neurocomputational operation (pattern completion-based retrieval) with a class of representational content (associative, high-dimensional memories). Because a full theory of memory must identify operations and representations separately, and specify how they interact, we argue that processes like recollection constitute inadequate labels for characterizing neural mechanisms. Instead, we advocate considering the component operations and representations of processes like recollection in isolation. For the organization of memory, the evidence suggests that pattern completion is recapitulated widely across the ventral visual stream and MTL, but the division of labor between sites within this pathway can be explained by representational content.

Visual perceptual decisions can be altered by recent experience. In the “serial dependence” effect, participants’ responses to visual stimuli appear to be biased toward (i.e., attracted to) recently encountered stimuli. Fischer and Whitney (2014) proposed that serial dependence reflects a “continuity field” that promotes visual stability by biasing perception toward the recent past. However, when participants are relatively accurate on the prior trial, there is no discernible difference between attraction to the prior stimulus and attraction to the prior response. To tease apart these alternative explanations of the attraction effect, we developed two complementary analysis techniques that rely on participants’ naturally occurring errors on a trial-by-trial basis, identifying any effect of the prior stimulus and, separately, any effect of the prior response (i.e., each effect could be attractive, repulsive, or absent). Applying these techniques to serial dependence data from a new experiment and four previously published studies, including Fischer and Whitney’s, we found that serial dependencies reflect an attraction to the previous response and repulsion from the previous stimulus, with these effects cancelling each other to different degrees for different experiments. In no case did we find evidence of an attraction to the prior stimulus. These results are consistent with literatures that predate the serial dependence effect: Attraction to prior responses is routinely observed in a wide variety of paradigms and repulsion from prior stimuli is ubiquitous, such as in the tilt aftereffect.

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The hippocampus is considered pivotal to recall, allowing retrieval of information not available in the immediate environment. In contrast, neocortex is thought to signal familiarity, contributing to recall only when called upon by the hippocampus. However, this view is not compatible with representational accounts of memory, which reject the mapping of cognitive processes onto brain regions. According to representational accounts, the hippocampus is not engaged by recall per se, rather it is engaged whenever hippocampal representations are required. To test whether hippocampus is engaged by recall when hippocampal representations are not required, we used functional imaging and a non-associative recall task, with images (objects, scenes) studied in isolation, and image patches as cues. As predicted by a representational account, hippocampal activation was modulated by the content of the recalled memory, increasing during recall of scenes-which are known to be processed by hippocampus-but not during recall of objects. Object recall instead engaged neocortical regions known to be involved in object-processing. Further supporting the representational account, effective connectivity analyses revealed that changes in functional activation during recall were driven by increased information flow from neocortical sites, rather than by the spreading of recall-related activation from hippocampus back to neocortex.

Damage to the medial temporal lobe (MTL) has long been known to impair declarative memory, and recent evidence suggests that it also impairs visual perception. A theory termed the representational-hierarchical account explains such impairments by assuming that MTL stores conjunctive representations of items and events, and that individuals with MTL damage must rely upon representations of simple visual features in posterior visual cortex, which are inadequate to support memory and perception under certain circumstances. One recent study of visual discrimination behavior revealed a surprising antiperceptual learning effect in MTL-damaged individuals: With exposure to a set of visual stimuli, discrimination performance worsened rather than improved [Barense, M. D., Groen, I. I. A., Lee, A. C. H., Yeung, L. K., Brady, S. M., Gregori, M., et al. Intact memory for irrelevant information impairs perception in amnesia. Neuron, 75, 157-167, 2012]. We extend the representational-hierarchical account to explain this paradox by assuming that difficult visual discriminations are performed by comparing the relative "representational tunedness"-or familiarity-of the to-be-discriminated items. Exposure to a set of highly similar stimuli entails repeated presentation of simple visual features, eventually rendering all feature representations maximally and, thus, equally familiar; hence, they are inutile for solving the task. Discrimination performance in patients with MTL lesions is therefore impaired by stimulus exposure. Because the unique conjunctions represented in MTL do not occur repeatedly, healthy individuals are shielded from this perceptual interference. We simulate this mechanism with a neural network previously used to explain recognition memory, thereby providing a model that accounts for both mnemonic and perceptual deficits caused by MTL damage with a unified architecture and mechanism.