It is well known that formation of new episodic memories depends on hippocampus, but in real-life settings (e.g., conversation), hippocampal amnesics can utilize information from several minutes earlier. What neural systems outside hippocampus might support this minutes-long retention? In this study, subjects viewed an audiovisual movie continuously for 25 min; another group viewed the movie in 2 parts separated by a 1-day delay. Understanding Part 2 depended on retrieving information from Part 1, and thus hippocampus was required in the day-delay condition. But is hippocampus equally recruited to access the same information from minutes earlier? We show that accessing memories from a few minutes prior elicited less interaction between hippocampus and default mode network (DMN) cortical regions than accessing day-old memories of identical events, suggesting that recent information was available with less reliance on hippocampal retrieval. Moreover, the 2 groups evinced
reliable but distinct DMN activity timecourses, reflecting differences in information carried in these regions when Part 1 was recent versus distant. The timecourses converged after 4 min, suggesting a time frame over which the continuous-viewing group may have relied less on hippocampal retrieval. We propose that cortical default mode regions can intrinsically retain real-life episodic information for several minutes.
Small changes in word choice can lead to dramatically different interpretations of narratives. How does the brain accumulate and integrate such local changes to construct unique neural representations for different stories? In this study we created two distinct narratives by changing only a few words in each sentence (e.g. “he” to “she” or “sobbing” to “laughing”) while preserving the grammatical structure across stories. We then measured changes in neural responses between the two stories. We found that the differences in neural responses between the two stories gradually increased along the hierarchy of processing timescales. For areas with short integration windows, such as early auditory cortex, the differences in neural responses between the two stories were relatively small. In contrast, in areas with the longest integration windows at the top of the hierarchy, such as the precuneus, temporal parietal junction, and medial frontal cortices, there were large differences in neural responses between stories. Furthermore, this gradual increase in neural difference between the stories was highly correlated with an area’s ability to integrate information over time. Amplification of neural differences did not occur when changes in words did not alter the interpretation of the story (e.g. “sobbing” to “crying”). Our results demonstrate how subtle differences in words are gradually accumulated and amplified along the cortical hierarchy as the brain constructs a narrative over time.
Antony, James W.; Cheng, Larry Y.; Brooks, Paula P.; Paller, Ken A.; Norman, Kenneth A.
Competition between memories can cause weakening of those memories. Here we investigated memory competition during sleep in human participants by presenting auditory cues that had been linked to two distinct picture-location pairs during wake. We manipulated competition during learning by requiring participants to rehearse picture-location pairs associated with the same sound either competitively (choosing to rehearse one over the other, leading to greater competition) or separately; we hypothesized that greater competition during learning would lead to greater competition when memories were cued during sleep. With separate-pair learning, we found that cueing benefited spatial retention. With competitive-pair learning, no benefit of cueing was observed on retention, but cueing impaired retention of well-learned pairs (where we expected strong competition). During sleep, post-cue beta power (16–30 Hz) indexed competition and predicted forgetting, whereas sigma power (11–16 Hz) predicted subsequent retention. Taken together, these findings show that competition between memories during learning can modulate how they are consolidated during sleep.
Pacheco, Diego A; Thiberge, Stephan; Pnevmatikakis, Eftychios; Murthy, Mala
Sensory pathways are typically studied starting at receptor neurons and following postsynaptic neurons into the brain. However, this leads to a bias in analysis of activity towards the earliest layers of processing. Here, we present new methods for volumetric neural imaging with precise across-brain registration, to characterize auditory activity throughout the entire central brain of Drosophila and make comparisons across trials, individuals, and sexes. We discover that auditory activity is present in most central brain regions and in neurons responsive to other modalities. Auditory responses are temporally diverse, but the majority of activity is tuned to courtship song features. Auditory responses are stereotyped across trials and animals in early mechanosensory regions, becoming more variable at higher layers of the putative pathway, and this variability is largely independent of spontaneous movements. This study highlights the power of using an unbiased, brain-wide approach for mapping the functional organization of sensory activity.
What mechanisms support our ability to estimate durations on the order of minutes? Behavioral studies in humans have shown that changes in contextual features lead to overestimation of past durations. Based on evidence that the medial temporal lobes and prefrontal cortex represent contextual features, we related the degree of fMRI pattern change in these regions with people's subsequent duration estimates. After listening to a radio story in the scanner, participants were asked how much time had elapsed between pairs of clips from the story. Our ROI analysis found that the neural pattern distance between two clips at encoding was correlated with duration estimates in the right entorhinal cortex and right pars orbitalis. Moreover, a whole-brain searchlight analysis revealed a cluster spanning the right anterior temporal lobe. Our findings provide convergent support for the hypothesis that retrospective time judgments are driven by 'drift' in contextual representations supported by these regions.
Bejjanki, Vikranth R.; da Silveira, Rava Azeredo; Cohen, Jonathan D.; Turk-Browne, Nicholas B.
Multivariate decoding methods, such as multivoxel pattern analysis (MVPA), are highly effective at extracting information from brain imaging data. Yet, the precise nature of the information that MVPA draws upon remains controversial. Most current theories emphasize the enhanced sensitivity imparted by aggregating across voxels that have mixed and weak selectivity. However, beyond the selectivity of individual voxels, neural variability is correlated across voxels, and such noise correlations may contribute importantly to accurate decoding. Indeed, a recent computational theory proposed that noise correlations enhance multivariate decoding from heterogeneous neural populations. Here we extend this theory from the scale of neurons to functional magnetic resonance imaging (fMRI) and show that noise correlations between heterogeneous populations of voxels (i.e., voxels selective for different stimulus variables) contribute to the success of MVPA. Specifically, decoding performance is enhanced when voxels with high vs. low noise correlations (measured during rest or in the background of the task) are selected during classifier training. Conversely, voxels that are strongly selective for one class in a GLM or that receive high classification weights in MVPA tend to exhibit high noise correlations with voxels selective for the other class being discriminated against. Furthermore, we use simulations to show that this is a general property of fMRI data and that selectivity and noise correlations can have distinguishable influences on decoding. Taken together, our findings demonstrate that if there is signal in the data, the resulting above-chance classification accuracy is modulated by the magnitude of noise correlations.
Rafidi, Nicole S; Hulbert, Justin C; Brooks, Paula P; Norman, Kenneth A
Repeated testing (as opposed to repeated study) leads to improved long-term memory retention, but the mechanism underlying this improvement remains controversial. In this work, we test the hypothesis that retrieval practice benefits subsequent recall by reducing competition from related memories. This hypothesis implies that the degree of reduction in competition between retrieval practice attempts should predict subsequent memory for the practiced items. To test this prediction, we collected electroencephalography (EEG) data across two sessions. In the first session, participants practiced selectively retrieving exemplars from superordinate semantic categories (high competition), as well as retrieving the names of the superordinate categories from exemplars (low competition). In the second session, participants repeatedly studied and were then tested on Swahili-English vocabulary. One week after session two, participants were again tested on the vocabulary. We trained a within-subject classifier on the data from session one to distinguish high and low competition states. We then used this classifier to measure competition across multiple retrieval practice attempts in the second session. The degree to which competition decreased for a given vocabulary word predicted whether that item was subsequently remembered in the third session. These results are consistent with the hypothesis that repeated testing improves retention by reducing competition.
Our daily lives revolve around sharing experiences and memories with others. When different people recount the same events, how similar are their underlying neural representations? In this study, participants viewed a fifty-minute audio-visual movie, then verbally described the events while undergoing functional MRI. These descriptions were completely unguided and highly detailed, lasting for up to forty minutes. As each person spoke, event-specific spatial patterns were reinstated (movie-vs.-recall correlation) in default network, medial temporal, and high-level visual areas; moreover, individual event patterns were highly discriminable and similar between people during recollection (recall-vs.-recall similarity), suggesting the existence of spatially organized memory representations. In posterior medial cortex, medial prefrontal cortex, and angular gyrus, activity patterns during recall were more similar between people than to patterns elicited by the movie, indicating systematic reshaping of percept into memory across individuals. These results reveal striking similarity in how neural activity underlying real-life memories is organized and transformed in the brains of different people as they speak spontaneously about past events.
This archive contains spike trains simultaneously recorded from ganglion cells in the tiger salamander retina with a multi-electrode array while viewing a repeated natural movie clip. These data have been analyzed in previous papers, notably Puchalla et al. Neuron 2005 and Schneidman et al. Nature 2006.
Recent advances in experimental techniques have allowed the simultaneous recordings of
populations of hundreds of neurons, fostering a debate about the nature of the collective
structure of population neural activity. Much of this debate has focused on the
empirical findings of a phase transition in the parameter space of maximum entropy
models describing the measured neural probability distributions, interpreting this phase
transition to indicate a critical tuning of the neural code. Here, we instead focus on the
possibility that this is a first-order phase transition which provides evidence that the
real neural population is in a `structured', collective state. We show that this collective
state is robust to changes in stimulus ensemble and adaptive state. We find that the
pattern of pairwise correlations between neurons has a strength that is well within the
strongly correlated regime and does not require fine tuning, suggesting that this state is
generic for populations of 100+ neurons. We find a clear correspondence between the
emergence of a phase transition, and the emergence of attractor-like structure in the
inferred energy landscape. A collective state in the neural population, in which neural
activity patterns naturally form clusters, provides a consistent interpretation for our
Extrapolation -- the ability to make inferences that go beyond the scope of one's experiences -- is a hallmark of human intelligence. By contrast, the generalization exhibited by contemporary neural network algorithms is largely limited to interpolation between data points in their training corpora. In this paper, we consider the challenge of learning representations that support extrapolation. We introduce a novel visual analogy benchmark that allows the graded evaluation of extrapolation as a function of distance from the convex domain defined by the training data. We also introduce a simple technique, context normalization, that encourages representations that emphasize the relations between objects. We find that this technique enables a significant improvement in the ability to extrapolate, considerably outperforming a number of competitive techniques.