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According to a “Swiss Army Knife” model of the brain, cognitive functions such as episodic memory and face perception map onto distinct neural substrates. In contrast, representational accounts propose that each brain region is best explained not by which specialized function it performs, but by the type of information it represents with its neural firing. In a functional magnetic resonance imaging study, we asked whether the neural signals supporting recognition memory fall mandatorily within the medial temporal lobes (MTL), traditionally thought the seat of declarative memory, or whether these signals shift within cortex according to the content of the memory. Participants studied objects and scenes that were unique conjunctions of pre-defined visual features. Next, we tested recognition memory in a task that required mnemonic discrimination of both simple features and complex conjunctions. Feature memory signals were strongest in posterior visual regions, declining with anterior progression toward the MTL, while conjunction memory signals followed the opposite pattern. Moreover, feature memory signals correlated with feature memory discrimination performance most strongly in posterior visual regions, whereas conjunction memory signals correlated with conjunction memory discrimination most strongly in anterior sites. Thus, recognition memory signals shifted with changes in memory content, in line with representational accounts. 

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 neurocomputationaloperation(pattern completion-based retrieval) with a class ofrepresentational 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. 

Normal aging impairs long-term declarative memory, and evidence suggests that this impairment may be driven partly by structural or functional changes in the medial temporal lobe (MTL). Theories of MTL memory function therefore make predictions for age-related memory loss. One theory – the Representational-Hierarchical account – makes two specific predictions. First, recognition memory performance in older participants should be impaired by feature-level interference, in which studied items contain many shared, and thus repeatedly appearing, perceptual features. Second, if the interference in a recognition memory task – i.e., the information that repeats across items – resides at a higher level of complexity than simple perceptual features, such as semantic gist, older adults should be less impacted by such interference than young adults. We tested these predictions using the Deese-Roediger-McDermott paradigm, by creating feature-level (i.e., perceptual) interference with phonemically/orthographically related word categories, and higher-level associative interference with semantically related word categories. We manipulated category size in order to compare the effect of less versus more interference (i.e., small versus large category size), which served to (1) avoid potential item confounds arising from systematic differences between words belonging to perceptually- versus semantically-related categories, and (2) ensure that any effect of interference was due to information encoded at study, rather than pre-experimentally. Further, we used signal detection theory (SDT) to interpret our data, rather than examining false alarm (FA) rates in isolation. The d’ measure derived from SDT avoids contamination of the memory measure by response bias, and theoretically lies on an interval scale, allowing memory performance in different conditions to be compared without violating assumptions of the statistical tests. Older participants were relatively more impaired by perceptual interference and less impaired by semantic interference than young adults. This pattern is at odds with many current theories of age-related memory loss, but is in line with the Representational-Hierarchical account. 

Identifying an object and distinguishing it from similar items depends upon the ability to perceive its component parts as conjoined into a cohesive whole, but the brain mechanisms underlying this ability remain elusive. The ventral visual processing pathway in primates is organized hierarchically: Neuronal responses in early stages are sensitive to the manipulation of simple visual features, whereas neuronal responses in subsequent stages are tuned to increasingly complex stimulus attributes. It is widely assumed that feature-coding dominates in early visual cortex whereas later visual regions employ conjunction-coding in which object representations are different from the sum of their simple feature parts. However, no study in humans has demonstrated that putative object-level codes in higher visual cortex cannot be accounted for by feature-coding and that putative feature codes in regions prior to ventral temporal cortex are not equally well characterized as object-level codes. Thus the existence of a transition from feature- to conjunction-coding in human visual cortex remains unconfirmed, and if a transition does occur its location remains unknown. By employing multivariate analysis of functional imaging data, we measure both feature-coding and conjunction-coding directly, using the same set of visual stimuli, and pit them against each other to reveal the relative dominance of one vs. the other throughout cortex. Our results reveal a transition from feature-coding in early visual cortex to conjunction-coding in both inferior temporal and posterior parietal cortices. This novel method enables the use of experimentally controlled stimulus features to investigate population-level feature and conjunction codes throughout human cortex. NEW & NOTEWORTHY We use a novel analysis of neuroimaging data to assess representations throughout visual cortex, revealing a transition from feature-coding to conjunction-coding along both ventral and dorsal pathways. Occipital cortex contains more information about spatial frequency and contour than about conjunctions of those features, whereas inferotemporal and parietal cortices contain conjunction coding sites in which there is more information about the whole stimulus than its component parts.