Biology subjects

Hayden, B.

Publications and source records attributed to Hayden, B..

At least 19 recordsLinked to original sources

bioRxiv2025

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↗

bioRxiv2025

The neural basis of emotional generalization in empathy

The essence of empathy is generalization of emotion across persons. Here, we leverage recent theoretical advances in the neuroscience of generalization to help us understand empathy. We measured brain activity in human neurosurgical patients performing two tasks, one focused on identifying their own emotional response and one identifying emotional responses in others. We quantified the representational geometry of local field potential (LFP) high-gamma activity in four regions: the medial temporal lobe, anterior cingulate cortex, orbitofrontal cortex, and insula. We found encoding of both self- and other-emotions in all four regions, but codes for emotion and person are disentangled (that is, factorized) in the insula, but not the other regions. This factorized representation allows for cross-person generalization of emotion in a way that tangled (non-factorized) representations do not. Together, these results support the hypothesis that the insula uniquely contributes to social mirroring processes by which we understand emotions across individuals.

neuroscience↗

bioRxiv2025

Human neuronal firing is modulated by the frequency of local field potential oscillations

Neural oscillations play a critical role in shaping neuronal firing patterns. While phase-locked neuronal firing ("phase tuning") has been extensively studied in animal models and human invasive recordings, much less is known about whether neurons show preferential firing at specific oscillatory frequencies, termed frequency tuning. Here, we employ human intracranial recordings across several brain regions including hippocampus, entorhinal cortex, anterior and posterior cingulate cortex, and orbitofrontal cortex to test the hypothesis that neurons exhibit frequency-specific firing. We analyzed 357 single units recorded simultaneously with local field potentials in 19 neurosurgical patients during awake resting. We estimated the instantaneous frequency of the LFP using adaptive spectral decomposition and assessed frequency tuning of each neuron while controlling for changes in firing rate unrelated to frequency changes. We found 27% neurons exhibited increased or decreased firing within specific frequencies, most commonly within the low-theta range (<10 Hz). Neurons exhibiting frequency tuning were distinct from those displaying phase tuning, and both types of tuning were observed across multiple brain regions with no anatomical preference. Together, our results demonstrate that the instantaneous frequency of neural oscillations modulates neuronal firing which may serve as an additional mechanism for information processing in the human brain, opening new avenues for frequency-targeted neural stimulation.

neuroscience↗

bioRxiv2025

Accumulation of virtual tokens towards a jackpot reward enhances performance and value encoding in dorsal anterior cingulate cortex

Normatively, our decisions ought to be made relative to our total wealth, but in practice, we make our decisions relative to variable, decision-time-specific set points. This predilection introduces a major behavior bias that is known as reference-point dependence in Prospect Theory, and that has close links to mental accounting. Here we examined neural activity in the dorsal anterior cingulate cortex (dACC) of macaques performing a token-based risky choice task, in which the acquisition of six tokens (accumulated over several trials) resulted in a jackpot reward. We find that subjects make faster and more accurate choices, and that they are less prone to risk-taking as offer contingencies are easier and the jackpot reward becomes more likely to be achieved. By comparing alternative models that accounted for progressive token accumulation, we found that subjective evaluations are best explained by a reference-dependent value RDV model where offer values are considered as potential gains or losses with respect to a token-dependent reference. The reference-dependent model allows to implement a dynamical comparison of the two offered values to each other and to the number of missing tokens to reach the six tokens threshold as jackpot approached. In dACC, we find that gains in subjective values entail higher fractions of encoding cells than losses, and that the encoding tuning of expected utility variables is best aligned to choices in gains than in losses. These results suggest a neural basis of reference dependence biases in shaping decision-making behavior and highlight the critical role of value representations in dACC in driving evaluations.

neuroscience↗

bioRxiv2025

Parietal cortex is recruited by frontal and cingulate areas to support action monitoring and updating during stopping

Recent evidence indicates that the intraparietal sulcus (IPS) may play a causal role in action stopping, potentially representing a novel neuromodulation target for inhibitory control dysfunctions. Here, we leverage intracranial recordings in human subjects to establish the timing and directionality of information flow between IPS and prefrontal and cingulate regions during action stopping. Prior to successful inhibition, information flows primarily from the inferior frontal gyrus (IFG), a critical inhibitory control node, to IPS. In contrast, during stopping errors the communication between IPS and IFG is lacking, and IPS is engaged by posterior cingulate cortex, an area outside of the classical inhibition network and typically associated with default mode. Anterior cingulate and orbitofrontal cortex also display performance-dependent connectivity with IPS. Our functional connectivity results provide direct electrophysiological evidence that IPS is recruited by frontal and anterior cingulate areas to support action plan monitoring/updating, and by posterior cingulate during control failures. In briefFunctional connectivity between the intraparietal sulcus (IPS) and a set of frontal and cingulate regions indicates that IPS is recruited to aid inhibitory control. Control failures are associated with increased communication with posterior cingulate. IPS could be a novel and tractable neuromodulation target for control-related neuropsychiatric disorders. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=107 SRC="FIGDIR/small/640787v1_ufig1.gif" ALT="Figure 1"> View larger version (35K): org.highwire.dtl.DTLVardef@e04699org.highwire.dtl.DTLVardef@3b1ea6org.highwire.dtl.DTLVardef@15961f4org.highwire.dtl.DTLVardef@12e144f_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LIParietal cortex displays performance-dependent activity in action stopping C_LIO_LIFunctional connectivity between IPS and IFG underlies successful stopping C_LIO_LIEarly communication from ACC and OFC to IPS is also specific to successful stopping C_LIO_LICommunication from PCC to IPS is higher during lapses in control C_LI

neuroscience↗

bioRxiv2025

A vectorial code for semantics in human hippocampus

As we listen to speech, our brains track the meanings of the words we hear. Recent successes of large language models suggest that distributed population geometry can capture rich semantic relationships between words. Motivated by this idea, we hypothesized that semantic information in the brain may likewise be expressed in distributed patterns of activity across neurons, rather than in the activity of neurons narrowly tuned to a specific word. We recorded responses of hundreds of neurons in the human hippocampus while participants listened to narrative speech. We find encoding of contextual word meaning in the simultaneous activity of neurons whose individual selectivities span multiple unrelated semantic categories. Decoding and population geometry analyses revealed distinct neural coding principles for low-versus high-frequency words, likely reflecting the greater polysemy of common words. Similar to embedding vectors in semantic language models, distance between neural population responses correlates with semantic distance; however, this effect was only observed in contextual embedding models (GPT-2 and BERT), suggesting that the semantic distance effect depends critically on contextualization. Consistent with this, we find that neural population activity supports a multidimensional semantic subspace that aligns most closely with the contextual structure captured by GPT-2. Moreover, for semantically similar words, even contextual embedders showed an inverse correlation between semantic and neural distances; we attribute this pattern to the noise-mitigating benefits of contrastive coding. Ultimately, these results provide a neurocomputational account for understanding how neural populations track word meaning.

neuroscience↗

bioRxiv2024

Control over a mixture of policies determines change of mind topology during continuous choice

Behavior is naturally organized into categorically distinct states with corresponding patterns of neural activity; how does the brain control those states? We propose that states are regulated by specific neural processes that implement meta-control that can blend simpler control processes. To test this hypothesis, we recorded from neurons in the dorsal anterior cingulate cortex (dACC) and dorsal premotor cortex (PMd) while macaques performed a continuous pursuit task with two moving prey that followed evasive strategies. We used a novel control theoretic approach to infer subjects moment-to-moment latent control variables, which in turn dictated their blend of distinct identifiable control processes. We identified low-dimensional subspaces in neuronal responses that reflected the current strategy, the value of the pursued target, and the relative value of the two targets. The top two principal components of activity tracked changes of mind in abstract and change-type-specific formats, respectively. These results indicate that control of behavioral state reflects the interaction of brain processes found in dorsal prefrontal regions that implement a mixture over low-level control policies.

neuroscience↗

bioRxiv2023

Gaze-centered gating and re-activation of value encoding in orbitofrontal cortex

During economic choice, we often consider options in alternation, until we commit to one. Nonetheless, neuroeconomics typically ignores the dynamic aspects of deliberation. We trained macaques to perform a value-based decision-making task where two risky offers were presented in sequence at different locations of the visual field, each followed by a delay epoch where offers were invisible. Subjects looked at the offers in sequence, as expected. Surprisingly, during the delay epochs, we found that subjects still tend to look at empty locations where the visual offers were formerly presented; and, moreover, longer fixation to given empty location increases the probability of choosing the associated offer, even after controlling for the offer values. We show that activity in orbitofrontal cortex (OFC) reflects the value of the gazed offer, but also the value of the offer associated to the gazed spatial location, even if it is not the most recently viewed. This reactivation reflects a reevaluation process, as fluctuations in neural spiking during offer stimuli presentation and delays correlate with upcoming choice. Our results suggest that look-at-nothing gazing triggers the reactivation of a previously seen offer for further reevaluation, revealing novel aspects of deliberation.

neuroscience↗

bioRxiv2023

Neural timescales reflect behavioral demands in freely moving rhesus macaques

Previous work has demonstrated remarkably reproducible and consistent hierarchies of neural timescales across cortical areas at rest. The question arises how such stable hierarchies give rise to adaptive behavior that requires flexible adjustment of temporal coding and integration demands. Potentially, this previously found lack of variability in the hierarchical organization of neural timescales could be a reflection of the structure of the laboratory contexts in which they were measured. Indeed, computational work demonstrates the existence of multiple temporal hierarchies within the same anatomical network when the input structure is altered. We posit that unconstrained behavioral environments where relatively little temporal demands are imposed from the experimenter are an ideal test bed to address the question of whether the hierarchical organization and the magnitude of neural timescales reflect ongoing behavioral demands. To tackle this question, we measured timescales of local field potential activity while rhesus macaques were foraging freely in a large open space. We find a hierarchy of neural timescales that is unique to this foraging environment. Importantly, although the magnitude of neural timescales generally expanded with task engagement, the brain areas relative position in the hierarchy was stable across the recording sessions. Notably, the magnitude of neural timescales monotonically expanded with task engagement across a relatively long temporal scale spanning the duration of the recording session. Over shorter temporal scales, the magnitude of neural timescales changed dynamically around foraging events. Moreover, the change in the magnitude of neural timescales contained functionally relevant information, differentiating between seemingly similar events in terms of motor demands and associated reward. That is, the patterns of change were associated with the cognitive and behavioral meaning of these events. Finally, we demonstrated that brain areas were differentially affected by these behavioral demands - i.e., the expansion of neural timescales was not the same across all areas. Together, these results demonstrate that the observed hierarchy of neural timescales is context-dependent and that changes in the magnitude of neural timescales are closely related to overall task engagement and behavioral demands.

neuroscience↗

bioRxiv2021

The PRO model accounts for the anterior cingulate cortex role in risky decision-making and monitoring

The anterior cingulate cortex (ACC) has been implicated in a number of functions including performance monitoring and decision making involving effort. The prediction of responses and outcomes (PRO) model has provided a unified account of much human and monkey ACC data involving anatomy, neurophysiology, EEG, fMRI, and behavior. Here we explore the computational nature of ACC with the PRO model, extending it to account specifically for both human and macaque monkey decision-making under risk, including both behavioral and neural data. We show that the PRO model can account for a number of additional effects related to outcome prediction, decision-making under risk, gambling behavior, and we show that the ACC represents the variance of uncertain outcomes, suggesting a link between ACC function and mean-variance theories of decision making. The PRO model provides a unified account of a large set of data regarding the ACC.

neuroscience↗

bioRxiv2021

Macaques preferentially attend to intermediately surprising information

Normative learning theories dictate that we should preferentially attend to informative sources, but only up to the point that our limited learning systems can process their content. Humans, including infants, show this predicted strategic deployment of attention. Here we demonstrate that rhesus monkeys, much like humans, attend to events of moderate surprisingness over both more and less surprising events. They do this in the absence of any specific goal or contingent reward, indicating that the behavioral pattern is spontaneous. We suggest this U-shaped attentional preference represents an evolutionarily preserved strategy for guiding intelligent organisms toward material that is maximally useful for learning.

animal behavior and cognition↗

bioRxiv2021

Pre-trial predictors of conflict response efficacy in human dorsolateral prefrontal cortex

The ability to perform motor actions depends, in part, on the brains initial state, that is, the ensemble firing rate pattern prior to the initiation of action. We hypothesized that the same principle would apply to cognitive functions as well. To test this idea, we examined a unique set of single unit data collected in human dorsolateral prefrontal (dlPFC) cortex. Data were collected in a conflict task that interleaves Simon (motor-type) and Eriksen (flanker-type) conflict trials. In dlPFC, variability in pre-trial firing rate predicted the ability to resolve conflict, as inferred from reaction times. Ensemble patterns that predicted faster Simon reaction times overlapped slightly with those predicting Erikson performance, indicating that the two conflict types are associated with near-orthogonal initial states, and suggesting that there is a weak abstract or amodal conflict preparatory state in this region. These codes became fully orthogonalized in the response state. We interpret these results in light of the initial state hypothesis, arguing that the firing patterns in dlPFC immediately preceding the start of a task predispose it for the efficient implementation of cognitive action.

neuroscience↗

bioRxiv2021

Subspace alignment as a mechanism for binding

To choose between options, we must solve two important binding problems. First, the features that determine each options values must be appropriately combined and kept separate from the corresponding features of other options. Second, options must be associated with the specific actions needed to select them. We hypothesized that the brain solves these problems through use of aligned (for bound dimensions) and orthogonal (for separated dimensions) population subspaces. We examined responses of single neurons in six putative value-coding regions in rhesus macaques performing a risky choice task. In all areas, single neurons encode the features that define the value of each option (stakes and probability) but only very weakly encode value per se. However, the coding dimensions associated with these features are aligned on a single subspace, from which a strong emergent value signal can be read out. Moreover, all six regions use nearly orthogonal subspaces for the left and right options, thereby linking options to their position in space, implementing functional partitioning, and reducing the possibility of misbinding. These results provide a new solution to the neuroeconomic binding problems and suggest that other forms of binding may work through similar principles.

neuroscience↗

bioRxiv2021

Distance decay 2.0 - a global synthesis of taxonomic and functional turnover in ecological communities.

Understanding the variation in community composition and species abundances, i.e., {beta}-diversity, is at the heart of community ecology. A common approach to examine {beta}-diversity is to evaluate directional turnover in community composition by measuring the decay in the similarity among pairs of communities along spatial or environmental distances. We provide the first global synthesis of taxonomic and functional distance decay along spatial and environmental distance by analysing 149 datasets comprising different types of organisms and environments. We modelled an exponential distance decay for each dataset using generalized linear models and extracted r2 and slope to analyse the strength and the rate of the decay. We studied whether taxonomic or functional similarity has stronger decay across the spatial and environmental distances. We also unveiled the factors driving the rate of decay across the datasets, including latitude, spatial extent, realm, and organismal features. Taxonomic distance decay was stronger along spatial and environmental distances compared with functional distance decay. The rate of taxonomic spatial distance decay was the fastest in the datasets from mid-latitudes while the rate of functional decay increased with latitude. Overall, datasets covering larger spatial extents showed a lower rate of decay along spatial distances but a higher rate of decay along environmental distances. Marine ecosystems had the slowest rate of decay. This synthesis is an important step towards a more holistic understanding of patterns and drivers of taxonomic and functional {beta}-diversity.

ecology↗

bioRxiv2021

Differential encoding of safe and risky offers

Common currency theories in neuroeconomics hold that neurons in specific brain regions specifically encode subjective values of offers and not stimulus-specific information. The rationale behind these theories is that abstract value encoding lets the decision maker compare qualitatively different options. Alternatively, expectancy-based theories hold that the brain preferentially tracks the relationship between options and their outcomes, and thus does not abstract away details of offers. To adjudicate between these theories, we examined responses of neurons in six reward regions to risky and safe offers while macaques performed a gambling task. In all regions, responses to safe options are unrelated to responses evoked by equally preferred risky options. Nor does any region appear to contain a specialized subset of value-selective neurons. Finally, in all regions, responses to risky and safe options occupy distinct response subspaces, indicating that the organizational framework for encoding risky and safe offers is different. Together, these results argue against the idea that putative reward regions carry abstract value signals, and instead support the idea that these regions carry information that links specific options to their outcomes in support of a broader cognitive map.

neuroscience↗

bioRxiv2020

Signatures of processing complexity during global cognitive states in ventromedial prefrontal cortex

Behavioral neuroscience almost exclusively studies behavior during tasks and ignores the unstructured inter-trial interval (ITI). However, it is unlikely that the ITI is simply an idling or paused mode; instead, it is a likely time for globally focused cognition, in which attention is disengaged from the task at hand and oriented more broadly. To gain insight into the computational underpinnings of globally focused cognition, we recorded from neurons in a core decision-making region, area 14 of ventromedial prefrontal cortex (vmPFC), as macaques performed a foraging search task with long inter-trial intervals (ITIs). We find that during the ITI, ensemble firing is associated with increased discriminability of a key mnemonic variable, recent reward rate, which in turn predicts upcoming search strategy. ITI activity is also associated with increased ensemble dimensionality and faster subspace reorganization, presumed markers of processing complexity. These results demonstrate the flexible nature of mnemonic processing and support the idea that the brain makes use of ostensible downtime to engage in complex processing.

animal behavior and cognition↗

bioRxiv2020

Anatomically distinct OFC-PCC circuits relay choice from value space to action space

Economic choice necessarily involves the transformation of abstract, object-based representations to concrete, action-based ones. This transformation is both determined and delimited by the neuroanatomical organization of the regions that implement it. In choice, the orbitofrontal cortex (OFC) plays a key role in both abstract valuation and cognitive mapping. However, determining the neural processes underlying this transformation has proven difficult. We hypothesized that difficulty stems from in part from the fact that the OFC consists of multiple functionally distinct zones that are distinguished by their differing contributions to the abstract-concrete transformation, and that these functions reflect their differing long-range projections. Here we identify two such subregions, defined by stronger or weaker bidirectional anatomical connectivity with the posterior cingulate cortex (PCC). We call these regions OFCin and OFCout, respectively. We find that OFCin, relative to OFCout, shows enhanced functional connectivity with PCC, as indicated by both spike-field coherence and mutual information. We find converging evidence that the OFCin-PCC circuit, but not the OFCout-PCC circuit, relays choice signals from an abstract value space to a concrete action space. Moreover, the OFCin-PCC circuit shows a putative bidirectional mutually excitatory pattern. Together, these results support the hypothesis that OFC-PCC subareal organization is critical for understanding the implementation of offer-action transformation in economic choice.

neuroscience↗

bioRxiv2020

Curiosity, latent learning, and cognitive maps

Curiosity refers to a desire for information that is not driven by immediate strategic or instrumental concerns. Latent earning refers to a form of learning that is not directly driven by standard reinforcement learning processes. We propose that curiosity serves the purpose of motivating latent learning. Thus, while latent learning is often treated as an incidental or passive process, in practice it most often reflects a strong evolved pressure to consume large amounts of information. That large volume of information in turn allows curious decision makers to generate sophisticated representations of the structure of their environment, known as cognitive maps. Cognitive maps facilitate adaptive and flexible behavior while maintaining its adaptivity and flexibility via map updates based on new information. Here we describe data supporting the idea that orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) play complementary roles in curiosity-driven learning. Specifically, we propose that (1) OFC tracks the innate value of information and incorporates new information into a detailed cognitive map; and (2) dACC tracks the environmental demands and information availability to then use the cognitive map for guiding behavior.

neuroscience↗