Cognitive strategies shift information from single neurons to populations in prefrontal cortex

Chiang, Feng-Kuei; Wallis, Jonathan D.; Rich, Erin L.

doi:10.1016/j.neuron.2021.11.021

Cited by 19 publications

(9 citation statements)

References 55 publications

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“…For decades, the dominant approach to understanding neural systems has been to characterize the role and contributions of individual neurons. In a recent paradigm shift, the concept of high-dimensional activity spaces that represent cognitive and other variables at the level of neuronal populations has taken the center stage and sidelined the single-neuron perspective (1)(2)(3). These population representations capture multineuron activity in different behavioral task conditions in the form of geometrical structures (4,5).…”

Section: Introductionmentioning

confidence: 99%

The neuronal implementation of representational geometry in primate prefrontal cortex

Lin,

Nieder,

Jacob

2023

Sci. Adv.

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Modern neuroscience has seen the rise of a population-doctrine that represents cognitive variables using geometrical structures in activity space. Representational geometry does not, however, account for how individual neurons implement these representations. Leveraging the principle of sparse coding, we present a framework to dissect representational geometry into biologically interpretable components that retain links to single neurons. Applied to extracellular recordings from the primate prefrontal cortex in a working memory task with interference, the identified components revealed disentangled and sequential memory representations including the recovery of memory content after distraction, signals hidden to conventional analyses. Each component was contributed by small subpopulations of neurons with distinct spiking properties and response dynamics. Modeling showed that such sparse implementations are supported by recurrently connected circuits as in prefrontal cortex. The perspective of neuronal implementation links representational geometries to their cellular constituents, providing mechanistic insights into how neural systems encode and process information.

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Section: Introductionmentioning

confidence: 99%

The neuronal implementation of representational geometry in primate prefrontal cortex

Lin,

Nieder,

Jacob

2023

Sci. Adv.

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“…On one extreme, the base unit of cognitive information is stored in a physical location, or engram, within an ensemble of cells that each have a dedicated contribution to the ensemble dynamics when activated 25 . On the other extreme, ensembles are functionalized through a population-level code where any given output can be achieved by distinct combinations of cellular members such that contributions of each are interchangeable, and no single component is indispensable 27,28 . In vivo recordings have demonstrated the existence and importance of ensembles in sensory and cognitive representations 29,30 ; however, at any given time, an unknown number of ensembles are active, due to encoding of sensory stimuli and internal cognitive processes which are constantly co-occurring in vivo .…”

Section: Resultsmentioning

confidence: 99%

“…Though the terminology has taken many forms over the decades, a repeated theme is whether networks of co-active cells, which we will refer to here as ensembles, are composed of dedicated versus labile members. Theories have spanned the spectrum of this dichotomy [25][26][27][28] . On one extreme, the base unit of cognitive information is stored in a physical location, or engram, within an ensemble of cells that each have a dedicated contribution to the ensemble dynamics when activated 25 .…”

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confidence: 99%

Recurrent activity within microcircuits of macaque dorsolateral prefrontal cortex tracks cognitive flexibility

Nolan,

Melugin,

Erickson

et al. 2023

Preprint

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Human and non–human primate data clearly implicate the dorsolateral prefrontal cortex (dlPFC) as critical for advanced cognitive functions1,2. It is thought that intracortical synaptic architectures within dlPFC are the integral neurobiological substrate that gives rise to these processes, including working memory, inferential reasoning, and decision–making3–7. In the prevailing model, each cortical column makes up one fundamental processing unit composed of dense intrinsic connectivity, conceptualized as the 'canonical' cortical microcircuit3,8. Each cortical microcircuit receives sensory and cognitive information from a variety of sources which are represented by sustained activity within the microcircuit, referred to as persistent or recurrent activity4,9. Via recurrent connections within the microcircuit, activity can propagate for a variable length of time, thereby allowing temporary storage and computations to occur locally before ultimately passing a transformed representation to a downstream output4,5,10. Competing theories regarding how microcircuit activity is coordinated have proven difficult to reconcilein vivowhere intercortical and intracortical computations cannot be fully dissociated5,9,11,12. Here, we interrogated the intrinsic features of isolated microcircuit networks using high–density calcium imaging of macaque dlPFCex vivo. We found that spontaneous activity is intrinsically maintained by microcircuit architecture, persisting at a high rate in the absence of extrinsic connections. Further, using perisulcal stimulation to evoke persistent activity in deep layers, we found that activity propagates through stochastically assembled intracortical networks, creating predictable population–level events from largely non–overlapping ensembles. Microcircuit excitability covaried with individual cognitive performance, thus anchoring heuristic models of abstract cortical functions within quantifiable constraints imposed by the underlying synaptic architecture.

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“…During social gaze interaction, individuals constantly evaluate objects and other individuals in the environment and make momentary decisions to look toward or away from them. OFC neurons encode a wide range of outcomerelated variables, such as expected value, choice value, reward prediction error, and choice and outcome history [32][33][34] that dynamically contribute to value and decision computations in OFC populations [35][36][37] . These decision computations in OFC might facilitate the encoding of moment-to-moment value associated with other's gaze and looking at other's eyes for guiding adaptive behaviors.…”

Section: Discussionmentioning

confidence: 99%

Closed-loop microstimulations of the orbitofrontal cortex during real-life gaze interaction enhance dynamic social attention

Fan,

Dal Monte,

Nair

et al. 2023

Preprint

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The prefrontal cortex is extensively involved in social exchange. During dyadic gaze interaction, multiple prefrontal areas exhibit neuronal encoding of social gaze events and context-specific mutual eye contact, supported by a widespread neural mechanism of social gaze monitoring. To explore causal manipulation of real-life gaze interaction, we applied weak closed-loop microstimulations that were precisely triggered by specific social gaze events to three prefrontal areas in monkeys. Microstimulations of orbitofrontal cortex (OFC), but not dorsomedial prefrontal or anterior cingulate cortex, enhanced momentary dynamic social attention in the spatial dimension by decreasing distance of one’s gaze fixations relative to partner monkey’s eyes. In the temporal dimension, microstimulations of OFC reduced the inter-looking interval for attending to another agent and the latency to reciprocate other’s directed gaze. These findings demonstrate that primate OFC serves as a functionally accessible node in controlling dynamic social attention and suggest its potential for a therapeutic brain interface.

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Cognitive strategies shift information from single neurons to populations in prefrontal cortex

Cited by 19 publications

References 55 publications

The neuronal implementation of representational geometry in primate prefrontal cortex

The neuronal implementation of representational geometry in primate prefrontal cortex

Recurrent activity within microcircuits of macaque dorsolateral prefrontal cortex tracks cognitive flexibility

Closed-loop microstimulations of the orbitofrontal cortex during real-life gaze interaction enhance dynamic social attention

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