bioRxiv Science⌕ Search

Biology subjects

Mickiewicz, E.

Publications and source records attributed to Mickiewicz, E..

11 recordsLinked to original sources

Estimation of neuronal tuning for word meaning from passively recorded naturalistic speech

The ability to derive neural-level language coding models holds great scientific and clinical potential. Current approaches are limited by the scale and ethological validity of input data; applications requiring large, rare, or naturalistic samples in particular would benefit from the ability to infer neural coding from incidental everyday speech. Here we present a novel pipeline designed to leverage spontaneous and incidental naturalistic speech. This pipeline performs transcription, segmentation, and video-assisted diarization, as well as alignment and spike detection of neural data. We apply this pipeline to a dataset derived from 21 patients (6+ days each, over 800 hours and 5 million words total). We benchmark both encoding and decoding models against extensive and rare ground-truth control datasets consisting of human-curated word-level temporal alignment and manually sorted spikes. We further validate our approach by quantifying representational drift, effect of dataset size, and differences between six brain areas. Together, these findings demonstrate that incidental natural speech is sufficiently processed in the brain to enable the estimation neural-level embeddings.

neuroscience↗

A number simplex in the human medial temporal lobe

Humans handle numbers nimbly, suggesting a richer neural manifold structure than the prevalent mental number line model. In populations of medial temporal lobe (MTL) neurons in humans performing two simple tasks (dot counting and arithmetic), we find robust neural coding of numerosity that results in high dimensional, simplex-shaped manifolds. This shape affords more flexibility than a linear manifold due to its high shattering dimensionality and expressibility. Dot arrays and Arabic numerals evoked distinct simplicial population codes, yet they were linked by a linearly transferable latent structure within the same task. We find similar simplicial geometry of number representations in large language models (LLMs). Moreover, subjects internally computed arithmetic results were decodable during the calculation period, with decoding accuracy correlating with individual mathematical capacity. Finally, linear transformations of simplicial operand representations modeled the brains conversion of operands into decodable results, suggesting that the brains arithmetic procedures have some resemblance to the attention architecture of LLMs. Together, these findings establish a high dimensional representational foundation for numerical cognition in the brain.

neuroscience↗

Polysemanticity in human hippocampal neurons

To comprehend language, the brain must navigate a high-dimensional semantic landscape while seamlessly contextualizing meaning. Inspired by recent advances in the mechanistic interpretability of large language models (LLMs), we hypothesized that the brain utilizes polysemanticity, a coding strategy wherein individual neurons represent multiple semantically unrelated features through high-dimensional superposition (Elhage et al., 2022; Olah et al., 2020). We recorded single-unit activity from the human hippocampus during podcast listening. We found that hippocampal neurons exhibit dense semantic codes characterized by multiple tuning peaks with an overdispersed, isotropic geometry. This geometry satisfies the theoretical requirements for interference minimization in superimposed codes. Furthermore, semantic responses are strongly modulated by lexical and speaker-identity context; nonetheless, the underlying population geometry remains stable. This coding strategy permits rapid contextualization without requiring specialized, context-specific neurons. Indeed, we show clear pattern separation of similar terms, along with pattern completion for held-out words. Together, these results demonstrate that the human brain leverages superposition to solve a universal computational problem: maximizing semantic capacity within a constrained representational space.

neuroscience↗

Distinct tasks engage a shared neural subspace in human hippocampus and anterior cingulate cortex

A hallmark of human cognitive flexibility is the ability to perform a wide range of unrelated tasks. While much is known about how neural circuits support individual tasks, less is understood about how these circuits support multiple tasks. Are neural representations largely task-specific, or do they retain a shared structure across distinct behaviors? To investigate this question, we recorded neural population activity from the hippocampus and anterior cingulate cortex, two regions linked to generalization and cognitive control, in eleven human patients performing three distinct tasks. Using dimensionality reduction, we estimated the neural subspace associated with each task and compared subspace geometry across tasks. We found that task-related subspaces were not independent: across tasks, approximately half of the subspace dimensions were shared, and these were primarily the dimensions containing most of the shared neural covariance. These findings indicate that neural population activity in these regions is not purely task-specific. This suggests a stable, low-dimensional circuit structure may persist even across unrelated behaviors, potentially providing a common substrate for flexible cognition.

neuroscience↗

Neural signatures of impaired semantic contextualization in Autism Spectrum Disorder

Social and communicative deficits are defining characteristics of autism spectrum disorder (ASD). Some theories suggest that these challenges, among other autistic traits, may arise from differences in predictive coding, or how the brain uses context to predict and interpret incoming information. This idea has the potential to link symptoms of autism to specific neurocomputational processes, and is especially promising for communication, whose impairment is a hallmark of ASD. Here we leveraged the ability of large language models (LLMs) to quantify semantic contextualization to analyze a unique dataset of responses from hippocampal neurons obtained during language listening in three mild-to-severe autistic individuals with comorbid epilepsy. Key elements of semantic coding were preserved in all three individuals with ASD: single-neuron response dynamics, representation of word-word semantic relationships, and patterns of context-dependent shifts in meaning. However, relative to controls, ASD resulted in reduced neural signatures of contextualization: (1) neuronal responses were aligned with earlier, less contextual layers of GPT-2, (2) ASD patients had lower effective dimensionality of the neural subspace predicting semantics, (3) neural representations of word meaning were less influenced by preceding context, and (4) neural signatures of lexical surprisal were reduced. Together, these results support theories of autism that emphasize impairments in contextualization, and highlight the power of LLMs as a tool for quantifying the computational basis of neurodevelopmental disorders.

neuroscience↗

Semantic axes in the brain support analogical representations

ABSTRACTIn language models of word meaning, directions in the embedding space often correspond to semantic features that can be reused across different words. For example, a single direction corresponding to gender may differentiate word pairs like "boy/girl", "uncle/aunt" and "king/queen". Here we show that the same principle governs semantically driven neural responses in the human brain. We recorded populations of single neurons during podcast listening and identified word sets with consistent meaning differences. Across fifteen sets, including gender, plural, and negation, we observed consistent vectorial directions, resulting in parallelogram structures within the neural manifold. Deviation from parallelism in large language models (LLMs) predicted corresponding deviations in brain-derived parallelism. Among pronouns, vectors corresponding to case, number and person exhibited parallelogram structures individually and, collectively, obeyed the principle of commutativity, resulting in a prismatic structure. Finally, different semantic variables were preferentially associated with discrete groups of neurons, consistent with energy-efficiency theories. Together, these results establish a geometric foundation for the neural encoding of word meaning.

neuroscience↗

Shared neural geometries for bilingual semantic representations

The human brain has the remarkable ability to comprehend and express similar concepts in multiple languages. To understand how it does so, we examined responses of hippocampal neurons during passive listening, directed speaking, and spontaneous conversation, in both English and Spanish, in a small group of balanced bilinguals. We find a small number of putative cross-language neurons, whose responses to equivalent words (e.g., "tierra" and "earth") are correlated. However, neurons semantic tunings differed substantially by language, suggesting language-specific neural implementations. Instead, the crucial driver of translation was a preserved geometric organization of neural responses between the two languages, one that did not depend on neuron level functional overlap. Indeed, that geometry was implemented by a common set of neurons along distinct readout axes; this difference in readout may help prevent cross-language interference. Together, these results suggest that hippocampus encodes a language-independent internal model for meaning.

neuroscience↗

A semantotopic map in human hippocampus

The hippocampus plays a central role in encoding abstract conceptual and semantic information. However, little is known about the topography of that encoding. We leveraged the rare opportunity to examine neural responses densely along a small portion of the human hippocampus, specifically, the mediolateral axis of the anterior body. We collected responses to passive language listening using Neuropixels probes in three anesthetized patients during clinically indicated neurosurgical procedures. We computed semantic tuning functions for each recording site by regressing threshold crossing events and single unit responses against semantic embeddings from GPT-2, Word2Vec, and SBERT. We find that tuning functions of more distant recording sites are more dissimilar, supporting the hypothesis semantotopic organization. Multiple semantic features showed systematic changes along that axis, including animacy, concreteness, and familiarity; notably, effects were individual-specific. Surprisingly, we also found a small but significant increase in semantic similarity as a function of distance between recording sites, on a shorter spatial scale, suggesting a modest periodic organization. Together, these results demonstrate the presence of a multiscale functional organization of semantics in the hippocampus.

neuroscience↗

Mirror manifolds: partially overlapping neural subspaces for speaking and listening

We utilize internal representations of meaning for two purposes: to understand the words we hear and to generate our own speech. This dual requirement necessitates abstract, modality-agnostic representations. Building on work identifying it as a hub for relational mapping, we hypothesized that the hippocampus supports abstract, cross-person representations, and uses shared semantic geometries to do so. We tested this hypothesis by examining hippocampal activity in a remarkable single-neuron dataset derived from conversational speech. Neurons robustly encoded meanings of both spoken and heard words, and used common geometric embeddings for both, leading to abstract meaning performance. Speaker identity was aligned with meaning via partial subspace alignment, which affords speaker-meaning binding by partitioning meaning by speaker while maintaining cross-speaker generalization. Degrees of subspace rotation varied on a single word level and depended systematically on semantic category. Together, these findings indicate how geometric principles allow for abstract cross-personal meanings while preserving binding to speaker identity.

neuroscience↗

Complementary roles for hippocampus and anterior cingulate in composing continuous choice

Naturalistic, goal directed behavior often requires continuous actions directed at dynamically changing goals. In this context, the closest analogue to choice is a strategic reweighting of multiple goal-specific control policies in response to shifting environmental pressures. To understand the algorithmic and neural bases of choice in continuous contexts, we examined behavior and brain activity in humans performing a continuous prey-pursuit task. Using a newly developed control-theoretic decomposition of behavior, we find pursuit strategies are well described by a meta-controller dictating a mixture of lower-level controllers, each linked to specific pursuit goals. We find that hippocampal neurons encode the policy blending variable in a value-invariant manner and monitor policy switches after they occur. ACC neurons encode policy switches in a value-dependent manner, with value related modulation detectable several hundred ms before the switch, alongside a ramping increase in mean firing rate toward the switch. Meanwhile, OFC activity is consistent with an encoding of the current value structure of the task, rather than policy switching. Together these results are consistent with a tripartite functional division in which hippocampus serves as a controller over behavior, ACC serves as a meta-controller, and OFC provides a value context signal. Overall, our results shed light onto the complex processes associated with choice during naturalistic continuous interactive behavior.

neuroscience↗

Independent Continuous Tracking of Multiple Agents in the Human Hippocampus

The pursuit of fleeing prey is a core element of many species behavioral repertoires. It poses the difficult problem of continuous tracking of multiple agents, including both self and others. To understand how this tracking is implemented neurally, we examined responses of hippocampal neurons while humans performed a joystick-controlled continuous prey-pursuit task involving two simultaneously fleeing prey (and, in some cases, a predator) in a virtual open field. We found neural maps encoding the positions of all the agents. All maps were multiplexed in single neurons and were disambiguated by the use of the population coding principle of semi-orthogonal subspaces, which can facilitate cross-agent generalization. Some neurons, more common in the posterior hippocampus, had narrow tuning functions reminiscent of place cells, lower firing rates, and high information per spike; others, which were found in both anterior and posterior hippocampus, had broad tuning functions, higher firing rates, and less information per spike. Semi-orthogonalization was selectively associated with the broadly tuned neurons. These results suggest an answer to the problem of navigational individuation, that is, how mapping codes can distinguish different agents, and establish the neuronavigational foundations of pursuit.

neuroscience↗