Tracking neural correlates of successful learning over repeated sequence observations

Abstract

The neural correlates of memory formation in humans have long been investigated by exposing subjects to diverse material and comparing responses to items later remembered to those forgotten. Tasks requiring memorization of sensory sequences afford unique possibilities for linking neural memorization processes to behavior, because, rather than comparing across different items of varying content, each individual item can be examined across the successive learning states of being initially unknown, newly learned, and eventually, fully known. Sequence learning paradigms have not yet been exploited in this way, however. Here, we analyze the event-related potentials of subjects attempting to memorize sequences of visual locations over several blocks of repeated observation, with respect to pre- and post-block recall tests. Over centro-parietal regions, we observed a rapid P300 component superimposed on a broader positivity, which exhibited distinct modulations across learning states that were replicated in two separate experiments. Consistent with its well-known encoding of surprise, the P300 deflection monotonically decreased over blocks as locations became better learned and hence more expected. In contrast, the broader positivity was especially elevated at the point when a given item was newly learned, i.e., started being successfully recalled. These results implicate the Broad Positivity in endogenously-driven, intentional memory formation, whereas the P300, in processing the current stimulus to the degree that it was previously uncertain, indexes the cumulative knowledge thereby gained. The decreasing surprise/P300 effect significantly predicted learning success both across blocks and across subjects. This presents a new, neural-based means to evaluate learning capabilities independent of verbal reports, which could have considerable value in distinguishing genuine learning disabilities from difficulties to communicate the outcomes of learning, or perceptual impairments, in a range of clinical brain disorders.

A resource for assessing information processing in the developing brain using EEG and eye tracking

“…The second paradigm involves the learning of simple sequences 6 . The third emulates a standard neuropsychological processing speed task, which involves multiple perceptual decisions, short-term memory, and motor responses.…”

A Resource for Assessing Information Processing in the Developing Brain Using EEG and Eye Tracking

“…The simplest paradigm permits the tracing of the three major processing stages for simple contrast decisions (O'Connell et al, 2012). The second paradigm involves the learning of simple sequences (Steinemann et al, 2016). The third emulates a standard neuropsychological processing speed task, which involves multiple perceptual decisions, short-term memory, and motor responses.…”

“…In order to evaluate the neural correlates of declarative learning, we included an explicit visual sequence learning paradigm, in which subjects repeatedly view a fixed sequence of flashed visual locations and attempt to memorize it in order to make regular intermediate recall reports. This task was originally developed by Moisello, Ghilardi and colleagues as a control condition for the examination of spectral EEG signatures of visuo-motor learning (Moisello et al, 2013), and was recently shown to be highly informative in its own right, in providing reliable indices of memory formation and surprise-modulated stimulus processing that related systematically to the ongoing progress of learning (Steinemann et al, 2016). An important aspect of the paradigm is that the information to be remembered (flashed location) is of the most elementary kind and computed very rapidly in the brain, so that perceptual decisions regarding the immediately presented item are completed quickly, allowing the longer-lasting neural signatures of memory formation to be reliably distinguished from the short-lived processes of immediate stimulus identification.…”

“…In the current task battery we employed an adapted version of the task of Steinemann et al (2016). Participants were asked to view a sequence of 10 flashed-circle stimuli, which appeared among 8 possible, marked locations on the screen.…”

“…Visual stimuli consisted of filled white circles with a diameter of 1 cm presented at eight different equidistant spatial locations on a radius of 5 cm eccentricity, and were continuously marked by static circular outlines (see Fig. 1 in (Steinemann et al, 2016). Stimuli were presented (and gradually faded out) for 200 ms, with an inter-stimulus interval of 1300 ms.…”