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  1. Article ; Online: Visuospatial information foraging describes search behavior in learning latent environmental features.

    Barack, David L / Bakkour, Akram / Shohamy, Daphna / Salzman, C Daniel

    Scientific reports

    2023  Volume 13, Issue 1, Page(s) 1126

    Abstract: In the real world, making sequences of decisions to achieve goals often depends upon the ability to learn aspects of the environment that are not directly perceptible. Learning these so-called latent features requires seeking information about them. ... ...

    Abstract In the real world, making sequences of decisions to achieve goals often depends upon the ability to learn aspects of the environment that are not directly perceptible. Learning these so-called latent features requires seeking information about them. Prior efforts to study latent feature learning often used single decisions, used few features, and failed to distinguish between reward-seeking and information-seeking. To overcome this, we designed a task in which humans and monkeys made a series of choices to search for shapes hidden on a grid. On our task, the effects of reward and information outcomes from uncovering parts of shapes could be disentangled. Members of both species adeptly learned the shapes and preferred to select tiles expected to be informative earlier in trials than previously rewarding ones, searching a part of the grid until their outcomes dropped below the average information outcome-a pattern consistent with foraging behavior. In addition, how quickly humans learned the shapes was predicted by how well their choice sequences matched the foraging pattern, revealing an unexpected connection between foraging and learning. This adaptive search for information may underlie the ability in humans and monkeys to learn latent features to support goal-directed behavior in the long run.
    MeSH term(s) Humans ; Learning ; Feeding Behavior ; Reward ; Choice Behavior
    Language English
    Publishing date 2023-01-20
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 2615211-3
    ISSN 2045-2322 ; 2045-2322
    ISSN (online) 2045-2322
    ISSN 2045-2322
    DOI 10.1038/s41598-023-27662-9
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  2. Article: The representational geometry of emotional states in basolateral amygdala.

    O'Neill, Pia-Kelsey / Posani, Lorenzo / Meszaros, Jozsef / Warren, Phebe / Schoonover, Carl E / Fink, Andrew J P / Fusi, Stefano / Salzman, C Daniel

    bioRxiv : the preprint server for biology

    2024  

    Abstract: Sensory stimuli associated with aversive outcomes cause multiple behavioral responses related to an animal's evolving emotional state, but neural mechanisms underlying these processes remain unclear. Here aversive stimuli were presented to mice, ... ...

    Abstract Sensory stimuli associated with aversive outcomes cause multiple behavioral responses related to an animal's evolving emotional state, but neural mechanisms underlying these processes remain unclear. Here aversive stimuli were presented to mice, eliciting two responses reflecting fear and flight to safety: tremble and ingress into a virtual burrow. Inactivation of basolateral amygdala (BLA) eliminated differential responses to aversive and neutral stimuli without eliminating responses themselves, suggesting BLA signals valence, not motor commands. However, two-photon imaging revealed that neurons typically exhibited mixed selectivity for stimulus identity, valence, tremble and/or ingress. Despite heterogeneous selectivity, BLA representational geometry was lower-dimensional when encoding valence, tremble and safety, enabling generalization of emotions across conditions. Further, tremble and valence coding directions were orthogonal, allowing linear readouts to specialize. Thus BLA representational geometry confers two computational properties that identify specialized neural circuits encoding variables describing emotional states: generalization across conditions, and readouts lacking interference from other readouts.
    Language English
    Publishing date 2024-04-21
    Publishing country United States
    Document type Preprint
    DOI 10.1101/2023.09.23.558668
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  3. Article ; Online: The contribution of nonhuman primate research to the understanding of emotion and cognition and its clinical relevance.

    Bernardi, Silvia / Salzman, C Daniel

    Proceedings of the National Academy of Sciences of the United States of America

    2019  Volume 116, Issue 52, Page(s) 26305–26312

    Abstract: Psychiatric disorders are often conceptualized as arising from dysfunctional interactions between neural systems mediating cognitive and emotional processes. Mechanistic insights into these interactions have been lacking in part because most work in ... ...

    Abstract Psychiatric disorders are often conceptualized as arising from dysfunctional interactions between neural systems mediating cognitive and emotional processes. Mechanistic insights into these interactions have been lacking in part because most work in emotions has occurred in rodents, often without concurrent manipulations of cognitive variables. Nonhuman primate (NHP) model systems provide a powerful platform for investigating interactions between cognitive operations and emotions due to NHPs' strong homology with humans in behavioral repertoire and brain anatomy. Recent electrophysiological studies in NHPs have delineated how neural signals in the amygdala, a brain structure linked to emotion, predict impending appetitive and aversive stimuli. In addition, abstract conceptual information has also been shown to be represented in the amygdala and in interconnected brain structures such as the hippocampus and prefrontal cortex. Flexible adjustments of emotional behavior require the ability to apply conceptual knowledge and generalize to different, often novel, situations, a hallmark example of interactions between cognitive and emotional processes. Elucidating the neural mechanisms that explain how the brain processes conceptual information in relation to emotional variables promises to provide important insights into the pathophysiology accounting for symptoms in neuropsychiatric disorders.
    Language English
    Publishing date 2019-12-23
    Publishing country United States
    Document type Journal Article
    ZDB-ID 209104-5
    ISSN 1091-6490 ; 0027-8424
    ISSN (online) 1091-6490
    ISSN 0027-8424
    DOI 10.1073/pnas.1902293116
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  4. Article: Abstract representations emerge in human hippocampal neurons during inference behavior.

    Courellis, Hristos S / Mixha, Juri / Cardenas, Araceli R / Kimmel, Daniel / Reed, Chrystal M / Valiante, Taufik A / Salzman, C Daniel / Mamelak, Adam N / Fusi, Stefano / Rutishauser, Ueli

    bioRxiv : the preprint server for biology

    2023  

    Abstract: Humans have the remarkable cognitive capacity to rapidly adapt to changing environments. Central to this capacity is the ability to form high-level, abstract representations that take advantage of regularities in the world to support ... ...

    Abstract Humans have the remarkable cognitive capacity to rapidly adapt to changing environments. Central to this capacity is the ability to form high-level, abstract representations that take advantage of regularities in the world to support generalization
    Language English
    Publishing date 2023-11-30
    Publishing country United States
    Document type Preprint
    DOI 10.1101/2023.11.10.566490
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  5. Article ; Online: Basolateral amygdala circuitry in positive and negative valence.

    O'Neill, Pia-Kelsey / Gore, Felicity / Salzman, C Daniel

    Current opinion in neurobiology

    2018  Volume 49, Page(s) 175–183

    Abstract: All organisms must solve the same fundamental problem: they must acquire rewards and avoid danger in order to survive. A key challenge for the nervous system is therefore to connect motivationally salient sensory stimuli to neural circuits that engage ... ...

    Abstract All organisms must solve the same fundamental problem: they must acquire rewards and avoid danger in order to survive. A key challenge for the nervous system is therefore to connect motivationally salient sensory stimuli to neural circuits that engage appropriate valence-specific behavioral responses. Anatomical, behavioral, and electrophysiological data have long suggested that the amygdala plays a central role in this process. Here we review experimental efforts leveraging recent technological advances to provide previously unattainable insights into the functional, anatomical, and genetic identity of neural populations within the amygdala that connect sensory stimuli to valence-specific behavioral responses.
    MeSH term(s) Animals ; Basolateral Nuclear Complex/cytology ; Basolateral Nuclear Complex/physiology ; Humans ; Nerve Net/physiology ; Reinforcement, Psychology
    Language English
    Publishing date 2018-03-08
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
    ZDB-ID 1078046-4
    ISSN 1873-6882 ; 0959-4388
    ISSN (online) 1873-6882
    ISSN 0959-4388
    DOI 10.1016/j.conb.2018.02.012
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  6. Article ; Online: Shared neural coding for social hierarchy and reward value in primate amygdala.

    Munuera, Jérôme / Rigotti, Mattia / Salzman, C Daniel

    Nature neuroscience

    2018  Volume 21, Issue 3, Page(s) 415–423

    Abstract: The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether ... ...

    Abstract The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank-which contributes to the assessment of the social value of individuals within a group-is linked in the amygdala to representations of rewards associated with nonsocial stimuli.
    MeSH term(s) Amygdala/physiology ; Animals ; Conditioning, Operant/physiology ; Hierarchy, Social ; Macaca mulatta ; Male ; Neurons/physiology ; Photic Stimulation ; Reward
    Language English
    Publishing date 2018-02-19
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 1420596-8
    ISSN 1546-1726 ; 1097-6256
    ISSN (online) 1546-1726
    ISSN 1097-6256
    DOI 10.1038/s41593-018-0082-8
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  7. Article ; Online: The Geometry of Abstraction in the Hippocampus and Prefrontal Cortex.

    Bernardi, Silvia / Benna, Marcus K / Rigotti, Mattia / Munuera, Jérôme / Fusi, Stefano / Salzman, C Daniel

    Cell

    2020  Volume 183, Issue 4, Page(s) 954–967.e21

    Abstract: The curse of dimensionality plagues models of reinforcement learning and decision making. The process of abstraction solves this by constructing variables describing features shared by different instances, reducing dimensionality and enabling ... ...

    Abstract The curse of dimensionality plagues models of reinforcement learning and decision making. The process of abstraction solves this by constructing variables describing features shared by different instances, reducing dimensionality and enabling generalization in novel situations. Here, we characterized neural representations in monkeys performing a task described by different hidden and explicit variables. Abstraction was defined operationally using the generalization performance of neural decoders across task conditions not used for training, which requires a particular geometry of neural representations. Neural ensembles in prefrontal cortex, hippocampus, and simulated neural networks simultaneously represented multiple variables in a geometry reflecting abstraction but that still allowed a linear classifier to decode a large number of other variables (high shattering dimensionality). Furthermore, this geometry changed in relation to task events and performance. These findings elucidate how the brain and artificial systems represent variables in an abstract format while preserving the advantages conferred by high shattering dimensionality.
    MeSH term(s) Animals ; Behavior, Animal ; Brain Mapping ; Computer Simulation ; Hippocampus/anatomy & histology ; Hippocampus/physiology ; Learning ; Macaca mulatta ; Male ; Models, Neurological ; Neural Networks, Computer ; Neurons/physiology ; Prefrontal Cortex/anatomy & histology ; Prefrontal Cortex/physiology ; Reinforcement, Psychology ; Task Performance and Analysis
    Language English
    Publishing date 2020-10-14
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
    ZDB-ID 187009-9
    ISSN 1097-4172 ; 0092-8674
    ISSN (online) 1097-4172
    ISSN 0092-8674
    DOI 10.1016/j.cell.2020.09.031
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  8. Article ; Online: Amygdala neural activity reflects spatial attention towards stimuli promising reward or threatening punishment.

    Peck, Christopher J / Salzman, C Daniel

    eLife

    2014  Volume 3

    Abstract: Humans and other animals routinely identify and attend to sensory stimuli so as to rapidly acquire rewards or avoid aversive experiences. Emotional arousal, a process mediated by the amygdala, can enhance attention to stimuli in a non-spatial manner. ... ...

    Abstract Humans and other animals routinely identify and attend to sensory stimuli so as to rapidly acquire rewards or avoid aversive experiences. Emotional arousal, a process mediated by the amygdala, can enhance attention to stimuli in a non-spatial manner. However, amygdala neural activity was recently shown to encode spatial information about reward-predictive stimuli, and to correlate with spatial attention allocation. If representing the motivational significance of sensory stimuli within a spatial framework reflects a general principle of amygdala function, then spatially selective neural responses should also be elicited by sensory stimuli threatening aversive events. Recordings from amygdala neurons were therefore obtained while monkeys directed spatial attention towards stimuli promising reward or threatening punishment. Neural responses encoded spatial information similarly for stimuli associated with both valences of reinforcement, and responses reflected spatial attention allocation. The amygdala therefore may act to enhance spatial attention to sensory stimuli associated with rewarding or aversive experiences.
    MeSH term(s) Action Potentials/physiology ; Amygdala/physiology ; Animals ; Appetite/physiology ; Attention/physiology ; Cues ; Fixation, Ocular/physiology ; Macaca mulatta ; Male ; Neurons/physiology ; Photic Stimulation ; Punishment ; Reward ; Space Perception/physiology ; Task Performance and Analysis
    Language English
    Publishing date 2014-10-30
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 2687154-3
    ISSN 2050-084X ; 2050-084X
    ISSN (online) 2050-084X
    ISSN 2050-084X
    DOI 10.7554/eLife.04478
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  9. Article ; Online: The amygdala and basal forebrain as a pathway for motivationally guided attention.

    Peck, Christopher J / Salzman, C Daniel

    The Journal of neuroscience : the official journal of the Society for Neuroscience

    2014  Volume 34, Issue 41, Page(s) 13757–13767

    Abstract: Visual stimuli associated with rewards attract spatial attention. Neurophysiological mechanisms that mediate this process must register both the motivational significance and location of visual stimuli. Recent neurophysiological evidence indicates that ... ...

    Abstract Visual stimuli associated with rewards attract spatial attention. Neurophysiological mechanisms that mediate this process must register both the motivational significance and location of visual stimuli. Recent neurophysiological evidence indicates that the amygdala encodes information about both of these parameters. Furthermore, the firing rate of amygdala neurons predicts the allocation of spatial attention. One neural pathway through which the amygdala might influence attention involves the intimate and bidirectional connections between the amygdala and basal forebrain (BF), a brain area long implicated in attention. Neurons in the rhesus monkey amygdala and BF were therefore recorded simultaneously while subjects performed a detection task in which the stimulus-reward associations of visual stimuli modulated spatial attention. Neurons in BF were spatially selective for reward-predictive stimuli, much like the amygdala. The onset of reward-predictive signals in each brain area suggested different routes of processing for reward-predictive stimuli appearing in the ipsilateral and contralateral fields. Moreover, neurons in the amygdala, but not BF, tracked trial-to-trial fluctuations in spatial attention. These results suggest that the amygdala and BF could play distinct yet inter-related roles in influencing attention elicited by reward-predictive stimuli.
    MeSH term(s) Amygdala/physiology ; Animals ; Attention/physiology ; Basal Forebrain/physiology ; Cues ; Electric Stimulation ; Emotions/physiology ; Functional Laterality/physiology ; Macaca mulatta ; Male ; Motivation/physiology ; Neural Pathways/physiology ; Photic Stimulation
    Language English
    Publishing date 2014-10-07
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 604637-x
    ISSN 1529-2401 ; 0270-6474
    ISSN (online) 1529-2401
    ISSN 0270-6474
    DOI 10.1523/JNEUROSCI.2106-14.2014
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  10. Article ; Online: Manipulating neural activity in physiologically classified neurons: triumphs and challenges.

    Gore, Felicity / Schwartz, Edmund C / Salzman, C Daniel

    Philosophical transactions of the Royal Society of London. Series B, Biological sciences

    2015  Volume 370, Issue 1677, Page(s) 20140216

    Abstract: Understanding brain function requires knowing both how neural activity encodes information and how this activity generates appropriate responses. Electrophysiological, imaging and immediate early gene immunostaining studies have been instrumental in ... ...

    Abstract Understanding brain function requires knowing both how neural activity encodes information and how this activity generates appropriate responses. Electrophysiological, imaging and immediate early gene immunostaining studies have been instrumental in identifying and characterizing neurons that respond to different sensory stimuli, events and motor actions. Here we highlight approaches that have manipulated the activity of physiologically classified neurons to determine their role in the generation of behavioural responses. Previous experiments have often exploited the functional architecture observed in many cortical areas, where clusters of neurons share response properties. However, many brain structures do not exhibit such functional architecture. Instead, neurons with different response properties are anatomically intermingled. Emerging genetic approaches have enabled the identification and manipulation of neurons that respond to specific stimuli despite the lack of discernable anatomical organization. These approaches have advanced understanding of the circuits mediating sensory perception, learning and memory, and the generation of behavioural responses by providing causal evidence linking neural response properties to appropriate behavioural output. However, significant challenges remain for understanding cognitive processes that are probably mediated by neurons with more complex physiological response properties. Currently available strategies may prove inadequate for determining how activity in these neurons is causally related to cognitive behaviour.
    MeSH term(s) Animals ; Behavior/physiology ; Brain/cytology ; Brain/physiology ; Conditioning (Psychology)/physiology ; Electrophysiological Phenomena ; Fear/physiology ; Fear/psychology ; Genetic Techniques ; Humans ; Learning/physiology ; Memory/physiology ; Neurons/classification ; Neurons/physiology ; Substance-Related Disorders/physiopathology ; Substance-Related Disorders/psychology
    Language English
    Publishing date 2015-05-08
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
    ZDB-ID 208382-6
    ISSN 1471-2970 ; 0080-4622 ; 0264-3839 ; 0962-8436
    ISSN (online) 1471-2970
    ISSN 0080-4622 ; 0264-3839 ; 0962-8436
    DOI 10.1098/rstb.2014.0216
    Database MEDical Literature Analysis and Retrieval System OnLINE

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