The medial temporal lobe (MTL) is traditionally considered to be a system that is specialized for long-term memory. Recent work has challenged this notion by demonstrating that this region can contribute to many domains of cognition beyond long-term memory, including perception and attention. One potential reason why the MTL (and hippocampus specifically) contributes broadly to cognition is that it contains relational representations—representations of multidimensional features of experience and their unique relationship to one another—that are useful in many different cognitive domains. Here, we explore the hypothesis that the hippocampus/MTL plays a critical role in attention and perception via relational representations. We compared human participants with MTL damage to healthy age- and education-matched individuals on attention tasks that varied in relational processing demands. On each trial, participants viewed two images (rooms with paintings). On “similar room” trials, they judged whether the rooms had the same spatial layout from a different perspective. On “similar art” trials, they judged whether the paintings could have been painted by the same artist. On “identical” trials, participants simply had to detect identical paintings or rooms. MTL lesion patients were significantly and selectively impaired on the similar room task. This work provides further evidence that the hippocampus/MTL plays a ubiquitous role in cognition by virtue of its relational and spatial representations and highlights its important contributions to rapid perceptual processes that benefit from attention.
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One-trial perceptual learning in the absence of conscious remembering and independent of the medial temporal lobe
A degraded, black-and-white image of an object, which appears meaningless on first presentation, is easily identified after a single exposure to the original, intact image. This striking example of perceptual learning reflects a rapid (one-trial) change in performance, but the kind of learning that is involved is not known. We asked whether this learning depends on conscious (hippocampus-dependent) memory for the images that have been presented or on an unconscious (hippocampus-independent) change in the perception of images, independently of the ability to remember them. We tested five memory-impaired patients with hippocampal lesions or larger medial temporal lobe (MTL) lesions. In comparison to volunteers, the patients were fully intact at perceptual learning, and their improvement persisted without decrement from 1 d to more than 5 mo. Yet, the patients were impaired at remembering the test format and, even after 1 d, were impaired at remembering the images themselves. To compare perceptual learning and remembering directly, at 7 d after seeing degraded images and their solutions, patients and volunteers took either a naming test or a recognition memory test with these images. The patients improved as much as the volunteers at identifying the degraded images but were severely impaired at remembering them. Notably, the patient with the most severe memory impairment and the largest MTL lesions performed worse than the other patients on the memory tests but was the best at perceptual learning. The findings show that one-trial, long-lasting perceptual learning relies on hippocampus-independent (nondeclarative) memory, independent of any requirement to consciously remember.
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- Award ID(s):
- 1926780
- NSF-PAR ID:
- 10275785
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 118
- Issue:
- 19
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- e2104072118
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Evidence that the hippocampus is critical for spatial memory in nonnavigational tests is mixed. A recent study reported that temporary hippocampal inactivation impaired spatial memory in the nonnavigational Hamilton Search Task in monkeys. However, several studies have documented no impairment on other nonnavigational spatial memory tests following permanent hippocampal lesions. It was hypothesized that transient, but not permanent, hippocampal disruption produces deficits because monkeys undergoing transient inactivation continue to try to use a hippocampal‐dependent strategy, whereas monkeys with permanent lesions use a nonhippocampal‐dependent strategy. We evaluated this hypothesis by testing five rhesus monkeys with hippocampal lesions and five controls on a computerized analogue of the Hamilton Search Task. On each trial, monkeys saw an array of squares on a touchscreen, each of which “hid” one reward. Retrieving a reward depleted that location and monkeys continued selecting squares until they found all rewards. The optimal strategy is to remember chosen locations and choose each square once. Unlike the inactivation study, monkeys with hippocampal damage were as accurate as controls regardless of retention interval. Critically, we found no evidence that the groups used different strategies, as measured by learning rates, spatial search biases, perseverative win‐stay errors, or inter‐choice distance. This discrepancy between the effect of inactivations and lesions may result from off‐target effects of inactivations or as‐yet‐unidentified differences between the physical and computerized tasks. Combined with previous evidence that hippocampal damage impairs navigational memory in monkeys, this evidence constrains the role of the hippocampus in spatial memory as being critical for navigational tests that likely involve allocentric spatial memory but not nonnavigational tests that likely involve egocentric spatial memory.
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ABSTRACT The medial temporal lobe (MTL) plays a critical role in episodic long‐term memory, but whether the MTL is necessary for visual short‐term memory is controversial. Some studies have indicated that MTL damage disrupts visual short‐term memory performance whereas other studies have failed to find such evidence. To account for these mixed results, it has been proposed that the hippocampus is critical in supporting short‐term memory for high resolution complex bindings, while the cortex is sufficient to support simple, low resolution bindings. This hypothesis was tested in the current study by assessing visual short‐term memory in patients with damage to the MTL and controls for high resolution and low resolution object‐location and object‐color associations. In the location tests, participants encoded sets of two or four objects in different locations on the screen. After each set, participants performed a two‐alternative forced‐choice task in which they were required to discriminate the object in the target location from the object in a high or low resolution lure location (i.e., the object locations were very close or far away from the target location, respectively). Similarly, in the color tests, participants were presented with sets of two or four objects in a different color and, after each set, were required to discriminate the object in the target color from the object in a high or low resolution lure color (i.e., the lure color was very similar or very different, respectively, to the studied color). The patients were significantly impaired in visual short‐term memory, but importantly, they were more impaired for high resolution object‐location and object‐color bindings. The results are consistent with the proposal that the hippocampus plays a critical role in forming and maintaining complex, high resolution bindings. © 2016 Wiley Periodicals, Inc.
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Abstract Monkeys with selective damage to the hippocampus are often unimpaired in matching‐to‐sample tests but are reportedly impaired in visual paired comparison. While both tests assess recognition of previously seen images, delayed matching‐to‐sample may engage active memory maintenance whereas visual paired comparison may not. Passive memory tests that are not rewarded with food and that do not require extensive training may provide more sensitive measures of hippocampal function. To test this hypothesis, we assessed memory in monkeys with hippocampal damage and matched controls by providing them the opportunity to repeatedly view small sets of videos. Monkeys pressed a button to play each video. The same 10 videos were used for six consecutive days, after which 10 new videos were introduced in each of seven cycles of testing. Our measure of memory was the extent to which monkeys habituated with repeated presentations, watching fewer videos per session over time. Monkeys with hippocampal lesions habituated more slowly than did control monkeys, indicating poorer memory for previous viewings. Both groups dishabituated each time new videos were introduced. These results, like those from preferential viewing, suggest that the hippocampus may be especially important for memory of incidentally encoded events.
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null (Ed.)Have you ever felt “groggy” after hitting your head? We are learning more about how important it is to protect your brain from injuries, such as concussion. Concussion is also called mild traumatic brain injury (mTBI). After an mTBI, most people think patients recover within a few weeks. We noticed that some college students who had had an mTBI were struggling to remember information for a few seconds. This ability is called working memory and we need it for most thinking jobs, like remembering the name of someone you just met, or what you wanted to get from the fridge. In our experiments, we tested different groups of students to see if they could remember things for 1 s, like the color of squares. Participants with a history of mTBI (on average, more than 4 years after injury) performed worse than students without a history of mTBI. The take-home message is that there can be lasting effects of mTBI, even years after it happens.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2104072118
