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Rust, N. C.

Publications and source records attributed to Rust, N. C..

8 recordsLinked to original sources

Neural representations of visual memory in inferotemporal cortex reveal a generalizable framework for translating between spikes and field potentials

Translating neurophysiological findings requires understanding the relationship between common measures of brain activity in animals (spiking activity) and humans (local field potentials, LFP). Prior work suggests alignment between population spiking and high-gamma activity (HGA, 50-150 Hz) of the LFP; however, this is not always observed and is consequently debated. Here, we show that this alignment and prior failures depend on the underlying coding scheme. First, we examined neural representations of variables related to visual memory in macaque inferotemporal cortex. We found that spikes and HGA were strikingly aligned for variables encoded as population response magnitude (novelty, recency, and memorability). However, a variable encoded as a distributed pattern of activity (category) was misaligned. Next, we showed that these insights generalize across many published studies, accounting for prior alignment successes and failures. These results provide a framework for translating between spikes and LFPs, highlighting the scenarios likely to be fruitful for translation.

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Resolving a paradox about how vision is transformed into familiarity

How is the act of seeing an image transformed into the memory that it has been seen? To investigate, we leveraged the systematic variation with which some images are better remembered than others, image memorability, to compare neural responses in inferotemporal cortex (ITC) and the hippocampus (HC) as macaque monkeys performed a single-exposure visual familiarity task. We found evidence for a two-stage algorithmic transformation from visual representations to familiarity, including a previously undescribed computational transformation of familiarity in the medial temporal lobe. At the first stage, more memorable images elicited more vigorous ITC firing-rate responses and stronger ITC familiarity signals (reflected as repetition suppression). This led to a counterintuitive intermingling of familiarity and memorability signals in ITC, but a representation that could be read out by a linear decoder. At the next stage, the medial temporal lobe selectively extracted ITC familiarity signals to produce a more isolated familiarity representation with minimal memorability modulation, reflected downstream in HC. These results shed light on how seeing is transformed into familiarity, and they establish the existence of a previously undescribed medial temporal lobe computation.

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Sharpened visual memory representations are reflected in inferotemporal cortex

Humans and other primates can robustly report whether theyve seen specific images before, even when those images are extremely similar to ones theyve previously seen. Multiple lines of evidence suggest that pattern separation computations in the hippocampus (HC) contribute to this behavior by shaping the fidelity of visual memory. However, unclear is whether HC uniquely determines memory fidelity or whether computations in other brain areas also contribute. To investigate, we recorded neural signals from inferotemporal cortex (ITC) and HC of two rhesus monkeys as they performed a memory task in which they judged whether images were novel or exactly repeated in the presence of visually similar lure images with a range of visual similarities. We found behavioral evidence for sharpening, reflected as memory performance that was nonlinearly transformed relative to a benchmark defined by visual representations in ITC. As expected, we found that behavioral sharpening aligned with visual memory representations in HC. Surprisingly, and unaccounted for by HC pattern separation proposals, we also found neural correlates of behavioral sharpening reflected in ITC. These results, coupled with further analysis of the data, suggest that ITC contributes to shaping the fidelity of visual memory in the transformation from visual processing to memory storage and signaling. SignificanceVisual recognition memories are stored with remarkable visual fidelity, allowing humans and other primates to distinguish images they have encountered from visually similar images they have not. This fidelity has long been attributed to computations in the hippocampus that sharpen visual representations before memory storage ("pattern separation"). Unclear is how this proposal aligns with other evidence that visual memories are stored within high-level visual cortex itself, before signals reach the hippocampus. Here we demonstrate that, like the hippocampus, inferotemporal cortex also reflects sharpened visual memory representations, suggesting that visual cortex contributes to shaping the visual fidelity of visual memory.

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The representation of mood in primate anterior insular cortex

Understanding how the brain reflects and shapes mood requires resolving the disconnect between behavioral measures of mood that can only be made in humans (typically based on subjective reports of happiness) and detailed measures of brain activity only available in animals. To achieve this, we developed a mood model to predict behavioral fluctuations in human subjective happiness as individuals experienced wins and losses during a gambling task. Next, we investigated how this operationalization of mood was reflected behaviorally and in the brains of two monkeys engaged in the same gambling task. We found a remarkable alignment between human mood model signatures, the impact of estimated mood on monkey choice, and the persistent responses of units in monkey anterior insular cortex -- including a matched timescale of integration across events. In comparison, the same signatures were only weakly reflected in lateral prefrontal cortex, suggesting that insular mood representations do not trivially follow from a signal broadcast to all higher brain areas. These results are consistent with a model in which the brain transforms experiences into mood by integrating events through a recurrently connected network of excitatory and inhibitory pools of neurons. These are among the first detailed insights into the nature of putative mood representations in the primate brain.

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Pinpointing the neural signatures of single-exposure visual familiarity

Memories of the images that we have seen are thought to be reflected in the reduction of neural responses in high-level visual areas such as inferotemporal (IT) cortex, a phenomenon known as repetition suppression (RS). We challenged this hypothesis with a task that required rhesus monkeys to report whether images were novel or repeated while ignoring variations in contrast, a stimulus attribute that is also known to modulate the overall IT response. The monkeys behavior was largely contrast-invariant, contrary to the predictions of an RS-inspired decoder, which could not distinguish responses to images that are repeated from those of lower contrast. However, the monkeys behavioral patterns were well-predicted by a linearly decodable variant in which the total spike count was corrected for contrast modulation. These results suggest that the IT neural activity pattern that best aligns with single-exposure visual recognition memory behavior is not RS but rather "sensory referenced suppression (SRS)": reductions in IT population response magnitude, corrected for sensory modulation. Significance statementMemories of whether an image has been seen before are reflected in high-level visual cortex as "sensory referenced suppression (SRS)": reductions in population response magnitude, corrected for sensory modulation.

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A neural correlate of image memorability

Some images are easy to remember while others are easily forgotten. While variation in image memorability is consistent across individuals, we lack a full account of its neural correlates. By analyzing data collected from inferotemporal cortex (IT) as monkeys performed a visual memory task, we demonstrate that a simple property of the visual encoding of an image, its population response magnitude, is strongly correlated with its memorability. These results establish a novel behavioral role for the magnitude of the IT response, which lies largely orthogonal to the coding scheme that IT uses to represent object identity. To investigate the origin of IT memorability modulation, we also probed convolutional neural network models trained to categorize objects. We found brain-analogous correlates of memorability that grew in strength across the hierarchy of these networks, suggesting that this memorability correlate is likely to arise from the optimizations required for visual as opposed to mnemonic processing.

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Single-exposure visual memory judgments are reflected in IT cortex

Our visual memory percepts of whether we have encountered specific objects or scenes before are hypothesized to manifest as decrements in neural responses in inferotemporal cortex (IT) with stimulus repetition. To evaluate this proposal, we recorded IT neural responses as two monkeys performed a single-exposure visual memory task designed to measure the rates of forgetting with time. We found that a weighted linear read-out of IT was a better predictor of the monkeys forgetting rates and reaction time patterns than a strict instantiation of the repetition suppression hypothesis, expressed as a total spike count scheme. Behavioral predictions could be attributed to visual memory signals that were reflected as repetition suppression and were intermingled with visual selectivity, but only when combined across the most sensitive neurons.

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Large nuisance modulation has little impact on IT target match performance

Finding a sought visual target object requires combining visual information about a scene with a remembered representation of the target to create a \"target match\" signal that indicates when a target is in view. Target match signals have been reported to exist within high-level visual brain areas including inferotemporal cortex (IT), where they are mixed with representations of image and object identity. However, these signals are not well understood, particularly in the context of the real-world challenge that the objects we search for typically appear at different positions, sizes, and within different background contexts. To investigate these signals, we recorded neural responses in IT as two rhesus monkeys performed a delayed-match-to-sample object search task in which target objects could appear at a variety of identity-preserving transformations. Consistent with the existence of behaviorally-relevant target match signals in IT, we found that IT contained a linearly separable target match representation that reflected behavioral confusions on trials in which the monkeys made errors. Additionally, target match signals were highly distributed across the IT population, and while a small fraction of units reflected target match signals as target match suppression, most units reflected target match signals as target match enhancement. Finally, we found that the potentially detrimental impact of target match signals on visual representations was mitigated by target match modulation that was approximately (albeit imperfectly) multiplicative. Together, these results support the existence of a robust, behaviorally-relevant target match representation in IT that is configured to minimally interfere with IT visual representations.

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