Theta phase precession supports memory formation and retrieval of naturalistic experience in humans.

Associating different aspects of experience with discrete events is critical for human memory. A potential mechanism for linking memory components is phase precession, during which neurons fire progressively earlier in time relative to theta oscillations. However, no direct link between phase precession and memory has been established. Here we recorded single-neuron activity and local field potentials in the human medial temporal lobe while participants (n = 22) encoded and retrieved memories of movie clips. Bouts of theta and phase precession occurred following cognitive boundaries during movie watching and following stimulus onsets during memory retrieval. Phase precession was dynamic, with different neurons exhibiting precession in different task periods. Phase precession strength provided information about memory encoding and retrieval success that was complementary with firing rates. These data provide direct neural evidence for a functional role of phase precession in human episodic memory.

Revealing Vision-Language Integration in the Brain with Multimodal Networks.

We use (multi)modal deep neural networks (DNNs) to probe for sites of multimodal integration in the human brain by predicting stereoen-cephalography (SEEG) recordings taken while human subjects watched movies. We operationalize sites of multimodal integration as regions where a multimodal vision-language model predicts recordings better than unimodal language, unimodal vision, or linearly-integrated language-vision models. Our target DNN models span different architectures (e.g., convolutional networks and transformers) and multimodal training techniques (e.g., cross-attention and contrastive learning). As a key enabling step, we first demonstrate that trained vision and language models systematically outperform their randomly initialized counterparts in their ability to predict SEEG signals. We then compare unimodal and multimodal models against one another. Because our target DNN models often have different architectures, number of parameters, and training sets (possibly obscuring those differences attributable to integration), we carry out a controlled comparison of two models (SLIP and SimCLR), which keep all of these attributes the same aside from input modality. Using this approach, we identify a sizable number of neural sites (on average 141 out of 1090 total sites or 12.94%) and brain regions where multimodal integration seems to occur. Additionally, we find that among the variants of multimodal training techniques we assess, CLIP-style training is the best suited for downstream prediction of the neural activity in these sites.

The Impact of Scene Context on Visual Object Recognition: Comparing Humans, Monkeys, and Computational Models.

During natural vision, we rarely see objects in isolation but rather embedded in rich and complex contexts. Understanding how the brain recognizes objects in natural scenes by integrating contextual information remains a key challenge. To elucidate neural mechanisms compatible with human visual processing, we need an animal model that behaves similarly to humans, so that inferred neural mechanisms can provide hypotheses relevant to the human brain. Here we assessed whether rhesus macaques could model human context-driven object recognition by quantifying visual object identification abilities across variations in the amount, quality, and congruency of contextual cues. Behavioral metrics revealed strikingly similar context-dependent patterns between humans and monkeys. However, neural responses in the inferior temporal (IT) cortex of monkeys that were never explicitly trained to discriminate objects in context, as well as current artificial neural network models, could only partially explain this cross-species correspondence. The shared behavioral variance unexplained by context-naive neural data or computational models highlights fundamental knowledge gaps. Our findings demonstrate an intriguing alignment of human and monkey visual object processing that defies full explanation by either brain activity in a key visual region or state-of-the-art models.

Neuron-level Prediction and Noise can Implement Flexible Reward-Seeking Behavior.

We show that neural networks can implement reward-seeking behavior using only local predictive updates and internal noise. These networks are capable of autonomous interaction with an environment and can switch between explore and exploit behavior, which we show is governed by attractor dynamics. Networks can adapt to changes in their architectures, environments, or motor interfaces without any external control signals. When networks have a choice between different tasks, they can form preferences that depend on patterns of noise and initialization, and we show that these preferences can be biased by network architectures or by changing learning rates. Our algorithm presents a flexible, biologically plausible way of interacting with environments without requiring an explicit environmental reward function, allowing for behavior that is both highly adaptable and autonomous. Code is available at https://github.com/ccli3896/PaN.

Feature-selective responses in macaque visual cortex follow eye movements during natural vision.

In natural vision, primates actively move their eyes several times per second via saccades. It remains unclear whether, during this active looking, visual neurons exhibit classical retinotopic properties, anticipate gaze shifts or mirror the stable quality of perception, especially in complex natural scenes. Here, we let 13 monkeys freely view thousands of natural images across 4.6 million fixations, recorded 883 h of neuronal responses in six areas spanning primary visual to anterior inferior temporal cortex and analyzed spatial, temporal and featural selectivity in these responses. Face neurons tracked their receptive field contents, indicated by category-selective responses. Self-consistency analysis showed that general feature-selective responses also followed eye movements and remained gaze-dependent over seconds of viewing the same image. Computational models of feature-selective responses located retinotopic receptive fields during free viewing. We found limited evidence for feature-selective predictive remapping and no viewing-history integration. Thus, ventral visual neurons represent the world in a predominantly eye-centered reference frame during natural vision.

Tuned Compositional Feature Replays for Efficient Stream Learning.

Our brains extract durable, generalizable knowledge from transient experiences of the world. Artificial neural networks come nowhere close to this ability. When tasked with learning to classify objects by training on nonrepeating video frames in temporal order (online stream learning), models that learn well from shuffled datasets catastrophically forget old knowledge upon learning new stimuli. We propose a new continual learning algorithm, compositional replay using memory blocks (CRUMB), which mitigates forgetting by replaying feature maps reconstructed by combining generic parts. CRUMB concatenates trainable and reusable memory block vectors to compositionally reconstruct feature map tensors in convolutional neural networks (CNNs). Storing the indices of memory blocks used to reconstruct new stimuli enables memories of the stimuli to be replayed during later tasks. This reconstruction mechanism also primes the neural network to minimize catastrophic forgetting by biasing it toward attending to information about object shapes more than information about image textures and stabilizes the network during stream learning by providing a shared feature-level basis for all training examples. These properties allow CRUMB to outperform an otherwise identical algorithm that stores and replays raw images while occupying only 3.6% as much memory. We stress-tested CRUMB alongside 13 competing methods on seven challenging datasets. To address the limited number of existing online stream learning datasets, we introduce two new benchmarks by adapting existing datasets for stream learning. With only 3.7%-4.1% as much memory and 15%-43% as much runtime, CRUMB mitigates catastrophic forgetting more effectively than the state-of-the-art. Our code is available at https://github.com/MorganBDT/crumb.git.

Minute-scale periodicity of neuronal firing in the human entorhinal cortex.

Grid cells in the entorhinal cortex demonstrate spatially periodic firing, thought to provide a spatial map on behaviorally relevant length scales. Whether such periodicity exists for behaviorally relevant time scales in the human brain remains unclear. We investigate neuronal firing during a temporally continuous experience by presenting 14 neurosurgical patients with a video while recording neuronal activity from multiple brain regions. We report on neurons that modulate their activity in a periodic manner across different time scales-from seconds to many minutes, most prevalently in the entorhinal cortex. These neurons remap their dominant periodicity to shorter time scales during a subsequent recognition memory task. When the video is presented at two different speeds, a significant percentage of these temporally periodic cells (TPCs) maintain their time scales, suggesting a degree of invariance. The TPCs' temporal periodicity might complement the spatial periodicity of grid cells and together provide scalable spatiotemporal metrics for human experience.

What is the intention to move and when does it occur?

In 1983 Benjamin Libet and colleagues published a paper apparently challenging the view that the conscious intention to move precedes the brain's preparation for movement. The experiment initiated debates about the nature of intention, the neurophysiology of movement, and philosophical and legal understanding of free will and moral responsibility. Here we review the concept of "conscious intention" and attempts to measure its timing. Scalp electroencephalographic activity prior to movement, the Bereitschaftspotential, clearly begins prior to the reported onset of conscious intent. However, the interpretation of this finding remains controversial. Numerous studies show that the Libet method for determining intent, W time, is not accurate and may be misleading. We conclude that intention has many different aspects, and although we now understand much more about how the brain makes movements, identifying the time of conscious intention is still elusive.

Neural coding: Stimulating cortex to alter visual perception.

A new study has shown that monkeys detect transient external pulses delivered to the highest echelons of visual cortex in a way that depends on concomitant visual inputs. This new work, a technical tour de force, has implications for the development of future visual prosthetic devices.

An adversarial collaboration protocol for testing contrasting predictions of global neuronal workspace and integrated information theory.

The relationship between conscious experience and brain activity has intrigued scientists and philosophers for centuries. In the last decades, several theories have suggested different accounts for these relationships. These theories have developed in parallel, with little to no cross-talk among them. To advance research on consciousness, we established an adversarial collaboration between proponents of two of the major theories in the field, Global Neuronal Workspace and Integrated Information Theory. Together, we devised and preregistered two experiments that test contrasting predictions of these theories concerning the location and timing of correlates of visual consciousness, which have been endorsed by the theories' proponents. Predicted outcomes should either support, refute, or challenge these theories. Six theory-impartial laboratories will follow the study protocol specified here, using three complementary methods: Functional Magnetic Resonance Imaging (fMRI), Magneto-Electroencephalography (M-EEG), and intracranial electroencephalography (iEEG). The study protocol will include built-in replications, both between labs and within datasets. Through this ambitious undertaking, we hope to provide decisive evidence in favor or against the two theories and clarify the footprints of conscious visual perception in the human brain, while also providing an innovative model of large-scale, collaborative, and open science practice.

Decoding of human identity by computer vision and neuronal vision.

Extracting meaning from a dynamic and variable flow of incoming information is a major goal of both natural and artificial intelligence. Computer vision (CV) guided by deep learning (DL) has made significant strides in recognizing a specific identity despite highly variable attributes. This is the same challenge faced by the nervous system and partially addressed by the concept cells-neurons exhibiting selective firing in response to specific persons/places, described in the human medial temporal lobe (MTL) ⁠. Yet, access to neurons representing a particular concept is limited due to these neurons' sparse coding. It is conceivable, however, that the information required for such decoding is present in relatively small neuronal populations. To evaluate how well neuronal populations encode identity information in natural settings, we recorded neuronal activity from multiple brain regions of nine neurosurgical epilepsy patients implanted with depth electrodes, while the subjects watched an episode of the TV series "24". First, we devised a minimally supervised CV algorithm (with comparable performance against manually-labeled data) to detect the most prevalent characters (above 1% overall appearance) in each frame. Next, we implemented DL models that used the time-varying population neural data as inputs and decoded the visual presence of the four main characters throughout the episode. This methodology allowed us to compare "computer vision" with "neuronal vision"-footprints associated with each character present in the activity of a subset of neurons-and identify the brain regions that contributed to this decoding process. We then tested the DL models during a recognition memory task following movie viewing where subjects were asked to recognize clip segments from the presented episode. DL model activations were not only modulated by the presence of the corresponding characters but also by participants' subjective memory of whether they had seen the clip segment, and by the associative strengths of the characters in the narrative plot. The described approach can offer novel ways to probe the representation of concepts in time-evolving dynamic behavioral tasks. Further, the results suggest that the information required to robustly decode concepts is present in the population activity of only tens of neurons even in brain regions beyond MTL.

Cross-task specificity and within-task invariance of cognitive control processes.

Cognitive control involves flexibly combining multiple sensory inputs with task-dependent goals during decision making. Several tasks involving conflicting sensory inputs and motor outputs have been proposed to examine cognitive control, including the Stroop, Flanker, and multi-source interference task. Because these tasks have been studied independently, it remains unclear whether the neural signatures of cognitive control reflect abstract control mechanisms or specific combinations of sensory and behavioral aspects of each task. To address these questions, we record invasive neurophysiological signals from 16 patients with pharmacologically intractable epilepsy and compare neural responses within and between tasks. Neural signals differ between incongruent and congruent conditions, showing strong modulation by conflicting task demands. These neural signals are mostly specific to each task, generalizing within a task but not across tasks. These results highlight the complex interplay between sensory inputs, motor outputs, and task demands underlying cognitive control processes.

LITTLE MEMORY EDITORS LIVING INSIDE YOUR BRAIN.

We interact with the world continuously. However, memories of our experiences are stored as individual events. For example, when we go on a road trip, we do not remember what happens second by second. Instead, we remember only a few special moments or events from a trip, such as dancing around the campfire. Our brains constantly extract memorable events while we interact with the world, and we organize those events based on their relevance. This process is like grouping road trip photos under different folders on the computer, so we can efficiently and accurately retrieve those memories in the future. How does the brain create these memorable events? In this article, you will learn about two groups of neurons inside the brain that help achieve this remarkable feat. You will also learn about how the activation of these neurons shapes the formation and retrieval of memories.

Learning to Learn: How to Continuously Teach Humans and Machines.

Curriculum design is a fundamental component of education. For example, when we learn mathematics at school, we build upon our knowledge of addition to learn multiplication. These and other concepts must be mastered before our first algebra lesson, which also reinforces our addition and multiplication skills. Designing a curriculum for teaching either a human or a machine shares the underlying goal of maximizing knowledge transfer from earlier to later tasks, while also minimizing forgetting of learned tasks. Prior research on curriculum design for image classification focuses on the ordering of training examples during a single offline task. Here, we investigate the effect of the order in which multiple distinct tasks are learned in a sequence. We focus on the online class-incremental continual learning setting, where algorithms or humans must learn image classes one at a time during a single pass through a dataset. We find that curriculum consistently influences learning outcomes for humans and for multiple continual machine learning algorithms across several benchmark datasets. We introduce a novel-object recognition dataset for human curriculum learning experiments and observe that curricula that are effective for humans are highly correlated with those that are effective for machines. As an initial step towards automated curriculum design for online class-incremental learning, we propose a novel algorithm, dubbed Curriculum Designer (CD), that designs and ranks curricula based on inter-class feature similarities. We find significant overlap between curricula that are empirically highly effective and those that are highly ranked by our CD. Our study establishes a framework for further research on teaching humans and machines to learn continuously using optimized curricula. Our code and data are available through this link.

Look twice: A generalist computational model predicts return fixations across tasks and species.

Primates constantly explore their surroundings via saccadic eye movements that bring different parts of an image into high resolution. In addition to exploring new regions in the visual field, primates also make frequent return fixations, revisiting previously foveated locations. We systematically studied a total of 44,328 return fixations out of 217,440 fixations. Return fixations were ubiquitous across different behavioral tasks, in monkeys and humans, both when subjects viewed static images and when subjects performed natural behaviors. Return fixations locations were consistent across subjects, tended to occur within short temporal offsets, and typically followed a 180-degree turn in saccadic direction. To understand the origin of return fixations, we propose a proof-of-principle, biologically-inspired and image-computable neural network model. The model combines five key modules: an image feature extractor, bottom-up saliency cues, task-relevant visual features, finite inhibition-of-return, and saccade size constraints. Even though there are no free parameters that are fine-tuned for each specific task, species, or condition, the model produces fixation sequences resembling the universal properties of return fixations. These results provide initial steps towards a mechanistic understanding of the trade-off between rapid foveal recognition and the need to scrutinize previous fixation locations.

Multiple transcription auto regulatory loops can act as robust oscillators and decision-making motifs.

Response time decides how fast a gene can react against an external signal at the transcription level in a signalling cascade. The steady state protein levels of the responding genes decide the coupling between two consecutive members of a signalling cascade. A negative autoregulatory loop (NARL) present in a transcription factor network can speed up the response time of the regulated gene at the cost of reduced steady state protein level. We present here a multi NARL motif which can be tuned for both the steady state protein level as well as response time in the required direction. Remarkably, there exists an optimum Hill coefficient nop t ≅ 4 at which the response time of the NARL motif is at minimum. When the Hill coefficient is n < nopt , then under strong binding conditions, one can raise the steady state protein level by increasing the gene copy number with almost no change in the response time of the multi NARL motif. Using detailed computational analysis, we show that the coupled multi NARL and positive auto regulatory loop (PARL) motifs can act as an oscillator as well as decision making component which are robust against extrinsic fluctuations in the control parameters. We further demonstrate that the period of oscillation of the coupled multi NARL-PARL dual feedback oscillator can also be fine-tuned by the gene copy number apart from the inducer concentration. We finally demonstrate robustness of bistable dual feedback decision making motifs with multi autoregulatory loop component.

Beyond the Cane: Describing Urban Scenes to Blind People for Mobility Tasks.

Blind people face difficulties with independent mobility, impacting employment prospects, social inclusion, and quality of life. Given the advancements in computer vision, with more efficient and effective automated information extraction from visual scenes, it is important to determine what information is worth conveying to blind travelers, especially since people have a limited capacity to receive and process sensory information. We aimed to investigate which objects in a street scene are useful to describe and how those objects should be described. Thirteen cane-using participants, five of whom were early blind, took part in two urban walking experiments. In the first experiment, participants were asked to voice their information needs in the form of questions to the experimenter. In the second experiment, participants were asked to score scene descriptions and navigation instructions, provided by the experimenter, in terms of their usefulness. The descriptions included a variety of objects with various annotations per object. Additionally, we asked participants to rank order the objects and the different descriptions per object in terms of priority and explain why the provided information is or is not useful to them. The results reveal differences between early and late blind participants. Late blind participants requested information more frequently and prioritized information about objects' locations. Our results illustrate how different factors, such as the level of detail, relative position, and what type of information is provided when describing an object, affected the usefulness of scene descriptions. Participants explained how they (indirectly) used information, but they were frequently unable to explain their ratings. The results distinguish between various types of travel information, underscore the importance of featuring these types at multiple levels of abstraction, and highlight gaps in current understanding of travel information needs. Elucidating the information needs of blind travelers is critical for the development of more useful assistive technologies.

Stochastic consolidation of lifelong memory.

Humans have the remarkable ability to continually store new memories, while maintaining old memories for a lifetime. How the brain avoids catastrophic forgetting of memories due to interference between encoded memories is an open problem in computational neuroscience. Here we present a model for continual learning in a recurrent neural network combining Hebbian learning, synaptic decay and a novel memory consolidation mechanism: memories undergo stochastic rehearsals with rates proportional to the memory's basin of attraction, causing self-amplified consolidation. This mechanism gives rise to memory lifetimes that extend much longer than the synaptic decay time, and retrieval probability of memories that gracefully decays with their age. The number of retrievable memories is proportional to a power of the number of neurons. Perturbations to the circuit model cause temporally-graded retrograde and anterograde deficits, mimicking observed memory impairments following neurological trauma.

Face neurons encode nonsemantic features.

The primate inferior temporal cortex contains neurons that respond more strongly to faces than to other objects. Termed "face neurons," these neurons are thought to be selective for faces as a semantic category. However, face neurons also partly respond to clocks, fruits, and single eyes, raising the question of whether face neurons are better described as selective for visual features related to faces but dissociable from them. We used a recently described algorithm, XDream, to evolve stimuli that strongly activated face neurons. XDream leverages a generative neural network that is not limited to realistic objects. Human participants assessed images evolved for face neurons and for nonface neurons and natural images depicting faces, cars, fruits, etc. Evolved images were consistently judged to be distinct from real faces. Images evolved for face neurons were rated as slightly more similar to faces than images evolved for nonface neurons. There was a correlation among natural images between face neuron activity and subjective "faceness" ratings, but this relationship did not hold for face neuron­evolved images, which triggered high activity but were rated low in faceness. Our results suggest that so-called face neurons are better described as tuned to visual features rather than semantic categories.