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.

A striking visual effect can be demonstrated by using a grayscale image of an object that has been degraded to a low-resolution, black-and-white image (1, 2). Such an image is difficult to identify (Fig. 1) but can be readily recognized after a single exposure to the original, intact image (Fig. 2) (3–6). Neuroimaging studies have found regions of the neocortex, including high-level visual areas and the medial parietal cortex, which exhibited a different pattern of activity when a degraded image was successfully identified (after seeing the intact image) than when the same degraded image was first presented and not identified (4, 5, 7). This phenomenon reflects a rapid change in performance based on experience, in this case one-trial learning, but the kind of learning that is involved is unclear.Open in a separate windowFig. 1.A sample degraded image. Most people cannot identify what is depicted. See Fig. 2.Open in a separate windowFig. 2.An intact version of the image in Fig. 1. When the intact version is presented just once directly after presentation of the degraded version, the ability to later identify the degraded image is greatly improved, even after many months. Reprinted from ref. (42), which is licensed under CC BY 4.0.One possibility is that successful identification of degraded images reflects conscious memory of having recently seen degraded images followed by their intact counterparts. When individuals see degraded images after seeing their “solutions,” they may remember what is represented in the images, at least for a time. In one study, performance declined sharply from 15 min to 1 d after the solutions were presented and then declined more gradually to a lower level after 21 d (3). Alternatively, the phenomenon might reflect a more automatic change in perception not under conscious control (8). Once the intact image is presented, the object in the degraded image may be perceived directly, independently of whether it is remembered as having been presented. By this account, successful identification of degraded images is reminiscent of the phenomenon of priming, whereby perceptual identification of words and objects is facilitated by single encounters with the same or related stimuli (9–11). Some forms of priming persist for quite a long time (weeks or months) (12–14).These two possibilities describe the distinction between declarative and nondeclarative memory (15, 16). Declarative memory affords the capacity for recollection of facts and events and depends on the integrity of the hippocampus and related medial temporal lobe structures (17, 18). Nondeclarative memory refers to a collection of unconscious memory abilities including skills, habits, and priming, which are expressed through performance rather than recollection and are supported by other brain systems (19–21). Does one-trial learning of degraded images reflect declarative or nondeclarative memory? How long does it last? In an early report that implies the operation of nondeclarative memory, two patients with traumatic amnesia improved the time needed to identify hidden images from 1 d to the next, but could not recognize which images they had seen (22). Yet, another amnesic patient reportedly failed such a task (23). The matter has not been studied in patients with medial temporal lobe (MTL) damage.To determine whether declarative (hippocampus-dependent) or nondeclarative (hippocampus-independent) memory supports the one-trial learning of degraded images, we tested five patients with bilateral hippocampal lesions or larger MTL lesions who have severely impaired declarative memory. The patients were fully intact at perceptual learning, and performance persisted undiminished from 1 d to more than 5 mo. At the same time, the patients were severely impaired at remembering both the structure of the test and the images themselves.