bioRxiv Science⌕ Search

Biology subjects

Kusunoki, M.

Publications and source records attributed to Kusunoki, M..

10 recordsLinked to original sources

Attentional selection drives information convergence within macaque lateral prefrontal cortex

Attention is a coherent state, in which multiple brain regions converge to represent selected features of a focal object or event. Lateral prefrontal cortex (LPFC), with its flexible coding of multiple task features and their conjunctions, is widely believed to play a key role in this process. While much research has investigated biased competition between features within a brain region, and cofluctuations of activity between regions, less is known about the representational dynamics through which a coherent neural state emerges. Here, we examine directed mutual information concerning multiple feature-specific population codes, between dorsal and ventral LPFC, across three phases of an attentional selection task. We find bidirectional convergence of information regarding multiple task features, but specifically following the period of selection from the visual display. The results show that neural processes driving inter-region coherence are especially salient during a period of cued object selection, despite comparable local information representation during other task phases. Significance statementIn the primate brain, lateral prefrontal cortex (LPFC) is thought to play a key role in selective attention, which is fundamental to goal-directed behaviour, and implies inter-region convergence towards a coherent representational state. Combining neural recordings, multivariate decoding, and analysis of information dynamics, we find local representations of multiple task features during multiple task phases, in separate regions of LPFC, with strong inter-region representational coherence emerging when attention could be directed to a chosen target. Results show that information convergence between these regions is bidirectional, sustained, and reflects multiple features of a chosen object, but, unlike local information representation, is highly specific to the choice phase of the task.

neuroscience↗

Neural dynamics in ventrolateral prefrontal cortex underlie learning from feedback

Learning often depends on feedback, yet how positive and negative outcomes reorganize target representations to support later memory retrieval remains poorly understood. Accumulating evidence suggests that the ventrolateral prefrontal cortex (vlPFC) acts as a central hub linking learning and retrieval, raising the possibility that it plays a critical role in this process. Here we analysed spiking activity and local field potentials (LFPs) recorded from vlPFC while monkeys performed a multi-cycle object-learning task. During the initial learning cycle, correct and incorrect feedback elicited distinct vlPFC neural responses in both spiking and LFPs. In particular, positive feedback produced elevated theta power and enhanced phase-amplitude coupling (PAC) between theta phase and high-frequency amplitude, associated with sustained suppression of neural spiking. Incorrect feedback induced stronger beta power. Despite comparable levels of object information under both feedback conditions, decoders trained and tested within the same feedback state outperformed those tested across states, revealing feedback-dependent coding formats. State-space and cross-period generalisation analyses further showed that object representations following positive feedback were geometrically closer to and shared a common coding format with those reinstated during later retrieval, indicating that feedback reshapes neural geometry toward retrieval-compatible states. Moreover, these geometric and generalisation effects were selectively expressed on electrodes showing stronger PAC or beta power, suggesting that oscillatory coordination may regulate how feedback signals are transformed into stable target codes. Together, our results reveal how vlPFC serves as a critical bridge between learning and memory retrieval, with feedback-driven dynamics reorganizing population geometry through rhythmic coordination and bringing successful outcome states closer to future retrieval representations.

neuroscience↗

Neural dynamics of an extended frontal lobe network in goal-subgoal problem solving

In goal-directed behavior, cognitive control calls for representation of current state, goal state, and current move, often with hierarchical organization into a series of steps or subgoals. In the human brain, a network of multiple-demand or MD regions underpins cognitive control, and core task features are likely encoded and integrated across this distributed network. Here we recorded from four putative homologs to human MD regions in the frontal cortex -- ventrolateral (vlPFC), dorsomedial (dmPFC), dorsal premotor (dPM) and anterior insula/orbitofrontal (I/O) cortex -- as two male monkeys solved a multi-step, on-screen spatial maze. Across regions there was substantial overlap but also wide quantitative variation in encoding task variables. Sensory input and current state were strongly coded in vlPFC, goal most stably in dmPFC, and move most rapidly in vlPFC and dPM. I/O responded during revision of a prepared route. In all regions, an abstract code of problem structure marked progress from problem start to end, with hierarchical separation of progress within and between successive steps. Partial specialisations, we suggest, arise from distinct connectivity, while broad co-recruitment reflects strong information exchange. Our results show how core components of goal-directed behavior are encoded across a distributed network of partial frontal lobe specialists, putatively homologous to frontal components of the human MD system.

neuroscience↗

Neural signatures for temporal-order memory in the medial posterior parietal cortex

Episodic memory involves encoding and remembering the order of events experienced over time. Previous work examining the mechanisms of temporal-order memories has focused on the hippocampus and prefrontal cortices but has largely ignored the memory ensembles in the medial posterior parietal cortex (mPPC). Combining in vivo multi-unit electrophysiology and a temporal-order judgment task with cinematic material in the macaque, we find that mPPC neuronal activity reflects temporal context both during encoding and recall. During learning, mPPC neuronal ensembles encode the temporal information as well as contextual information embedded in the videos, whereas at retrieval these neurons fire in synchrony prior to memory-guided decisions. Moreover, the similarity between encoding and retrieval correlates with the animals performance. A control experiment further ruled out eye saccades, fixation, and scan path for their confounding roles in the neural results. Together, these data suggest that neurons in mPPC track the passage of time and contextual changes, thereby orchestrating for successful temporal-order memories at retrieval. SIGNIFICANCERemembering the temporal order of events is a vital function of the brain. This study provides the first evidence for the retrieval of temporal order of episodes at both single neuron and ensemble levels in the primate parietal cortex. The studys key breakthrough is the revelation that ensembles of time perceptive neurons, acting as "temporal context cells", can encode a spectrum of time constants and contexts for the experienced past and subsequently utilize this temporal record to discriminate the chronological order of past experiences. These results enhance theoretical frameworks for how encoded temporal past is maintained and reconstructed during memory retrieval.

neuroscience↗

Ignorance is bliss: effects of noise and metaboliccost on cortical task representations

Cognitive flexibility requires both the encoding of task-relevant and the ignoring of task-irrelevant stimuli. While the neural coding of task-relevant stimuli is increasingly well understood, the mechanisms for ignoring task-irrelevant stimuli remain poorly understood. Here, we study how task performance and biological constraints jointly determine the coding of relevant and irrelevant stimuli in neural circuits. Using mathematical analyses and task-optimized recurrent neural networks, we show that neural circuits can exhibit a range of representational geometries depending on the strength of neural noise and metabolic cost. By comparing these results with recordings from primate prefrontal cortex (PFC) over the course of learning, we show that neural activity in PFC changes in line with a minimal representational strategy. Specifically, our analyses reveal that the suppression of dynamically irrelevant stimuli is achieved by activity-silent, sub-threshold dynamics. Our results provide a normative explanation as to why PFC implements an adaptive, minimal representational strategy.

neuroscience↗

Mixed selectivity coding of content-temporal detail by dorsomedial posterior parietal neurons

The dorsomedial posterior parietal cortex is part of a higher-cognition network implicated in elaborate processes underpinning memory formation, recollection, episodes reconstruction, and temporal information processing. Neural coding for complex episodic processing is however under-documented. Here we revealed a set of neural codes of neuroethogram in the primate parietal cortex. Analyzing neural responses in macaque dmPPC to naturalistic videos, we discovered several groups of neurons that are sensitive to different categories of ethogram-items and to low-level sensory features, and saccadic eye movement. We also discovered that the processing of category and feature information by these neurons is sustained by accumulation of temporal information over a long timescale up to 30 s, corroborating its reported long temporal receptive windows. We performed an additional behavioral experiment and found that saccade-related activities could not account for the mixed neuronal responses elicited by the video stimuli. We further observed monkeys scan-paths and gaze consistency are modulated by video content. Taken altogether, these neural findings explain how dorsomedial PPC weaves fabrics of ongoing experiences together in real-time. The high dimensionality of neural representations should motivate us to shift the focus of attention from pure selectivity neurons to mixed selectivity neurons, especially in increasingly complex naturalistic task designs. HIGHLIGHTSO_LINeural codes for "neuroethogram" in macaque dorsomedial parietal cortex C_LIO_LIParietal neural codes exhibit mixed selectivity of event features C_LIO_LIDorsomedial PPC neurons support a long temporal receptive window for episodes C_LIO_LISaccadic movement could not explain away mixed neuronal responses C_LIO_LIConsistency in scan-path and gaze shown across viewing repetitions C_LI

neuroscience↗

A one-shot learning signal in monkey prefrontal cortex

Much animal learning is slow, with cumulative changes in behavior driven by reward prediction errors. When the abstract structure of a problem is known, however, both animals and formal learning models can rapidly attach new items to their roles within this structure, sometimes in a single trial. Frontal cortex is likely to play a key role in this process. To examine information seeking and use in a known problem structure, we trained monkeys in a novel explore/exploit task, requiring the animal first to test objects for their association with reward, then, once rewarded objects were found, to re-select them on further trials for further rewards. Many cells in the frontal cortex showed an explore/exploit preference, changing activity in a signal trial to align with one-shot learning in the monkeys behaviour. In contrast to this binary switch, these cells showed little evidence of continuous changes linked to expectancy or prediction error. Explore/exploit preferences were independent for two stages of the trial, object selection and receipt of feedback. Within an established task structure, frontal activity may control the separate operations of explore and exploit, switching in one trial between the two. Significance statementMuch animal learning is slow, with cumulative changes in behavior driven by reward prediction errors. When the abstract structure a problem is known, however, both animals and formal learning models can rapidly attach new items to their roles within this structure. To address transitions in neural activity during one-shot learning, we trained monkeys in an explore/exploit task using familiar objects and a highly familiar task structure. In contrast to continuous changes reflecting expectancy or prediction error, frontal neurons showed a binary, one-shot switch between explore and exploit. Within an established task structure, frontal activity may control the separate operations of exploring alternative objects to establish their current role, then exploiting this knowledge for further reward.

neuroscience↗

Prefrontal neural dynamics for behavioral decisions and attentional control

Complex neural dynamics in the prefrontal cortex contribute to context-dependent decisions and attentional competition. To analyze these dynamics, we apply demixed principal component analysis to activity of a primate prefrontal cell sample recorded in a cued target detection task. The results track dynamics of cue and object coding, feeding into movements along a target present-absent decision axis in a low-dimensional subspace of population activity. For a single stimulus, object and cue coding are seen mainly in the contralateral hemisphere. Later, a developing decision code in both hemispheres may reflect interhemispheric communication. With a target in one hemifield and a competing nontarget in the other, each hemisphere initially encodes the contralateral object, but finally, decision coding is dominated by the task-relevant target. These findings further suggest that exchange of information between hemispheres plays a key role when attentional competition resolves. Tracking complex neural events in a low-dimensional activity subspace illuminates integration of neural codes towards task-appropriate behavior, comprising a building block of learned task structure in the prefrontal cortex. AUTHOR SUMMARYFlexible adaptive processing of information is integral for everyday goal-directed behavior. To unravel dynamic representation of task-relevant information, we analyzed population activity of a primate prefrontal cell sample in a cued target detection task. In a low-dimensional neural subspace, with separate axes for cue, object identity and decision, trajectories showed initial coding of cue and object in the contralateral hemisphere, followed by coding of the behavioral decision across both hemispheres. With target and nontarget stimuli in opposite hemifields, the data suggest initial coding of the contralateral object in each hemisphere. Object coding is then rapidly shut off for the nontarget, and followed by bilateral coding of the target decision. The results bring detailed insight into task structure and information flow within and between the two frontal lobes as a decision is made and attentional competition is resolved.

neuroscience↗

Distinguishing between parallel and serial processing in visual attention from neurobiological data

Serial and parallel processing in visual search have been long debated in psychology but the processing mechanism remains an open issue. Serial processing allows only one object at a time to be processed, whereas parallel processing assumes that various objects are processed simultaneously. Here we present novel neural models for the two types of processing mechanisms based on analysis of simultaneously recorded spike trains using electrophysiological data from prefrontal cortex of rhesus monkeys while processing task-relevant visual displays. We combine mathematical models describing neuronal attention and point process models for spike trains. The same model can explain both serial and parallel processing by adopting different parameter regimes. We present statistical methods to distinguish between serial and parallel processing based on both maximum likelihood estimates and decoding the momentary focus of attention when two stimuli are presented simultaneously. Results show that both processing mechanisms are in play for the simultaneously recorded neurons, but neurons tend to follow parallel processing in the beginning after the onset of the stimulus pair, whereas they tend to serial processing later on. This could be explained by parallel processing being related to sensory bottom-up signals or feedforward processing, which typically occur in the beginning after stimulus onset, whereas top-down signals related to cognitive modulatory influences guiding attentional effects in recurrent feedback connections occur after a small delay, and is related to serial processing, where all processing capacities are being directed towards the attended object.\n\nAuthor summaryA fundamental question concerning processing of visual objects in our brain is how a population of cortical cells respond when presented with more than a single object in their receptive fields. Is one object processed at a time (serial processing), or are all objects processed simultaneously (parallel processing)? Inferring the dynamics of attentional states in simultaneously recorded spike trains from sensory neurons while being exposed to a pair of visual stimuli is key to advance our understanding of visual cognition. We propose novel statistical models and measures to quantify and follow the time evolution of the visual cognition processes right after stimulus onset. We find that in the beginning processing appears to be predominantly parallel, which develops into serial processing 150 - 200 ms after stimulus onset in prefrontal cortex of rhesus monkeys.

neuroscience↗

Propofol induces metabolic reprogramming and cell death in a mitochondrial electron transport chain-dependent manner

The intravenous anesthetic propofol (2,6-diisopropylphenol) has been used for the induction and maintenance of anesthesia in operating rooms and for sedation in intensive care units. Although there is no widely accepted definition of propofol infusion syndrome (PRIS), PRIS is defined as the development of metabolic acidosis, rhabdomyolysis, hyperkalemia, hepatomegaly, renal failure, arrhythmia, and progressive cardiac failure. In vitro evidence suggests that PRIS is related to the impaired mitochondrial function. There are indications that preexisting mitochondrial disorders predispose to PRIS. However, the precise molecular mechanisms, including mitochondrial defects and a metabolic conversion by propofol, are largely unknown as yet. To elucidate the underlying cellular and molecular mechanisms of PRIS, we investigated the effects of propofol on the cellular metabolic mode and cell death. We demonstrated that clinically relevant concentrations of propofol, used within a clinically relevant exposure time, suppressed the mitochondrial function, caused the generation of reactive oxygen species, and induced a metabolic switch, from oxidative phosphorylation to glycolysis, by targeting complexes I and III of mitochondria. The data also indicated that a predisposition to mitochondrial dysfunction, caused by a genetic mutation or pharmacological suppression of the electron transport chain by biguanides such as metformin and phenformin, promoted the cell death and caspase activation induced by propofol.

pharmacology and toxicology↗