Sensations in action : how behavioural context affects sensory information processing ? / Les sensations en action: comment le contexte comportemental affecte-t-il le traitement de l’information sensorielle?

Seminar organized by Nathalie Rochefort and Brice Bathellier from April 10 to 15, 2023.

Participants

Mark ANDERMANN (Beth Israel Deaconess Medical Center, Center for Life Sciences – BOSTON, États-Unis), Sophie BAGUR (Institut de l’audition – Paris, France), Brice BATHELLIER (Institut Pasteur – CNRS UMR3691 – Paris, France), Jennifer BIZLEY (University College London – London, Royaume-Uni), Solange BROWN (Johns Hopkins University School of Medicine – Baltimore, MD, Étas-Unis), Jessica CARDIN (Yale University – New Haven, États-Unis), Robert FROEMKE (New York University Grossman School of Medicine – New York, États-Unis), Georg KELLER (Friedrich Miescher Institute – Basel, Suisse), Máté LENGYEL (University of Cambridge – Cambridge, Royaume-Uni), Zhang LI (Keck School of Medicine of Usc – Los Angeles, États-Unis), Janelle PAKAN (Otto von Guericke University Magdeburg – Magdeburg, Allemagne), Jonathan PILLOW (Princeton University – Princeton, États-Unis), Beatriz RICO (King’s College London – London , Royaume-Uni), Nathalie ROCHEFORT (University of Edinburgh – Edinburgh, Royaume-Uni), Pieter ROELFSEMA (Netherlands Institute for Neurosciences – Amsterdam, Pays-Bas), Massimo SCANZIANI (UCSF and HHMI – San Francisco, États-Unis), David SCHNEIDER (New York University Grossman School of Medicine – New York, États-Unis).

Summary

We perceive our body and environment through sensory receptors sending information to central sensory systems in the brain. Although sensory systems are classically described as circuits dedicated to the processing of sensory information, a wide range of evidence indicates that sensory signals coexist with a rich contextual information, particularly in the cortical sensory regions. This contextual information includes multisensory information, body and brain states as well as predictions from past experiences.The neuroscience community is heavily debating on the mechanisms underlying the integration of these inputs with sensory information. This includes deciphering what information is actually read-out by downstream targets of sensory cortices, and how this plays a role in computing behaviourally relevant responses, given the diversity of ecological constraints, behaviors and brain architectures across species.

This seminar gathered 17 neuroscientists including two junior researchers, bringing together experts from different fields which to date have had limited interactions: from molecular and cellular biology, to neuronal circuit anatomy and function, computational modeling and machine learning. We discussed how the recurrent functional architecture of sensory cortex and its interplay with subcortical circuits convey and integrate contextual information, generate different brain states and compute expectations of sensory signals. Present and future methodological developments were discussed, ranging from computational approaches aimed at modeling behavior to potential avenues for unraveling the role of combinatorial hormonal and neuromodulatory signaling. We identified key questions and principles regarding the integration of contextual information with sensory inputs and the generation of internal models of behavioral interactions with the environment. We received unanimous positive feedback from the participants; the interactions that arose from this seminar promise to produce long-lasting and fruitful collaborations among the participants.

Résumé 

Nous percevons notre corps et notre environnement grâce à des récepteurs sensoriels qui relaient l’information sensorielle aux systèmes sensoriels centraux situés dans le cerveau. Bien que les systèmes sensoriels soient classiquement décrits comme des circuits dédiés au traitement des informations sensorielles, un large éventail de preuves indique que les signaux sensoriels coexistent avec une riche information contextuelle, en particulier dans les régions sensorielles corticales. Cette information contextuelle inclut des informations multisensorielles, des informations sur le comportement et l’état interne de l’animal ainsi que des prédictions basées sur des expériences passées. La communauté des neurosciences débat vigoureusement à propos des mécanismes sous-jacents à l’intégration de cette information contextuelle avec les inputs sensoriels. Cela inclut le décodage des informations reçues par les régions du cerveau en aval des cortex sensoriels, et comment cela influence la génération de réponses comportementalement pertinentes, étant donné la diversité des contraintes écologiques, des comportements et des architectures cérébrales chez différentes espèces.

Ce séminaire a rassemblé 17 neuroscientifiques, dont deux chercheurs juniors, réunissant des experts de différents domaines qui ont jusqu’à présent eu des interactions limitées : de la biologie moléculaire et cellulaire, à l’anatomie des circuits neuronaux, la neurophysiologie fonctionnelle, la modélisation computationnelle et l’intelligence artificielle. Nous avons discuté de la façon dont l’architecture fonctionnelle récurrente du cortex sensoriel et son interaction avec les circuits sous-corticaux transmettent et intègrent l’information contextuelle avec les signaux sensoriels, et génèrent ainsi des modèles internes et des prédictions de l’environnement sensoriel externe. Les recherches en cours de nouvelles méthodes ont été soulignées, allant des méthodes computationnelles visant à modéliser le comportement aux approches moléculaires pour décoder le rôle de la signalisation hormonale et neuromodulatrice. Nous avons identifié des mécanismes et des questions clés concernant l’intégration de l’information contextuelle avec les entrées sensorielles et la génération de modèles internes d’interactions comportementales avec l’environnement. Les interactions qui ont découlé de ce séminaire ont été unanimement saluées par les participants comme fructueuses et source d’inspiration pour leur recherches futures et promettent de produire des collaborations durables et fructueuses entre les participants.

Report

The brain processes sensory information to generate sensations, thoughts and motor actions that integrate into complex and dynamic behavioural contexts. This process involves the integration of sensory inputs with internal information about the behavioural-state and behavioral context of the animal as well as with internal models generated from previous experiences associated with similar sensory inputs. A long-lasting question in neuroscience is to understand how the brain combines such diverse internal and external information to produce contextually adapted behaviors.

In mammals, the neocortex is undoubtedly a key circuit for this process: it integrates sensory information, computes decisions, elaborates actions and contributes to memories of past events, based on a seemingly stereotypical architecture of six layers, highly recurrent connections within and outside the cortical network, and diverse modulations by neuromodulatory and hormonal signaling. As a result of this recurrent connectivity, the information encoded in the cortex is extremely rich and diverse, not only in the areas described as associative. A large number of recent results indeed indicate that an important property of the primary sensory cortex is the ability to integrate different sources of sensory and non-sensory information in order to generate flexible representations of the sensory environment to drive appropriate behaviors. These non-sensory signals include responses to motor movements, speed, arousal, reward, internal information related to the metabolic and hormonal state of the animal (e.g. hunger, pregnancy) as well as expectations generated from past experiences associated with specific sensory stimuli.

The main goal of this seminar was to discuss the origin of contextual signals in sensory cortex and the possible mechanisms underlying the integration of these inputs with sensory information. This includes deciphering what information is actually read-out by downstream targets of primary sensory cortices, and how this plays a role in computing behaviourally relevant responses, given the diversity of ecological constraints and behaviors.

This seminar was hosted by the Fondation les Treilles from April 10-15, 2023, bringing together 17 investigators from Europe and North America, each of whom were experts in sensory information processing but came from diverse fields that typically have limited interaction: from molecular and cellular biology, to neuronal circuit anatomy and function, computational modeling and machine learning. The seminar was organized around 4 sessions with interactive talks and extensive discussions. Each session included 2 to 4 individual talks (1 hour-long) and a general discussion. The discussions were organized around 4 themes: (1) cortico-subcortical loops in sensory processing; (2) neuronal basis of conscious/non-consious perception; (3) neuromodulatory and hormonal influence on sensory perception; (4) internal models and predictive coding.

We explored how the diversity of information processed in primary sensory areas is conveyed through reciprocal cortico-cortical circuits and their relation with subcortical structures such as the thalamus (Solange Brown, Massimo Scanziani, Li Zhang, Sophie Bagur), the claustrum (Solange Brown), the cerebellum (Janelle Pakan) and hypothalamic nuclei (Li Zhang; Robert Froemke). The presentations by Georg Keller, Beatriz Rico, Solange Brown, and Li Zhang highlighted specific circuits that connect different cortical layers with key cortical and subcortical pathways related to learnt or innate behaviors. This precise connectivity within the cerebral cortex is established during development through distinct molecular mechanisms underlying the formation of cell-type specific synaptic connections between inhibitory and excitatory neurons (Beatriz Rico).

Our discussions converged on the idea that a critical function of this architecture is to build an internal representation of the environment which can efficiently interact with internal states and motor plans to drive appropriate behaviors. In this respect, the talks of Pieter Roelfsema, Georg Keller, Jennifer Bizley, Janelle Pakan, Sophie Bagur and David Schneider gave concrete examples about the content of internal models, the neuronal implementation of these representations, and their coupling with on-going motor actions, both in the auditory and the visual systems. Such internal models in auditory cortex included self-awareness of self-generated sounds (David Schneider) and invariant representations of sound location (Jennifer Bizley), while in the visual cortex, internal models were investigated in the context of circuits underlying visuo-motor integration based on self-generated movements (Georg Keller). An emerging theme of the discussions was the role of cortex in sensory-motor actions. While simple learning of a basic stimulus-action association does not necessarily require specific processing by cortical circuits, the integration of information over time, from short-time scales to the detection of longer term regularities, appeared to be a key function of the cortical circuits, as shown during the presentations by Sophie Bagur and Pieter Roefselma.

The activation of such systems may contribute to what is described as the conscious access to information, which remains one of the most mysterious functions of the cortex. The question of the mechanisms that may underlie conscious versus unconscious access to sensory information was addressed by several talks, analyzing (1) how the information about consciously reported visual stimuli evolve at successive stages from the visual to the frontal cortex (Pieter Roelfsema), (2) how ‘offline’ stimulus reactivations occur in the visual cortex during hippocampal sharp-wave ripples (Mark Andermann), (3) how rapid eye movements during REM sleep reveal the direction and amplitude of the ongoing changes in the thalamic head direction system, thereby providing a window into the cognitive processes of the sleeping brain (Massimo Scanziani) and, finally, (4) how under anesthesia, a state without conscious access in humans, the structure of sensory representations in cortex is widely changed and drastically reduces the coexistence of distinct information flows (Brice Bathellier).

The cortex is therefore a highly dynamic circuit that can change its operating mode based on behavioral constraints. Computational modeling was presented to be a powerful approach to characterize states both at the neuronal and behavioral level and quantify hypotheses about the computations performed in different states as advocated by Máté Lengyel and Jonathan Pillow in their presentations. The talks by Jessica Cardin and Mark Anderman highlighted neuronal circuits underlying these dynamics and the crucial role of neuromodulation in behavioral state transitions. In addition to neuromodulation, hormones also have a profound impact on sensory information processing. Two presentations showed that physiological constraints signaled by hormones have a strong and long lasting effect in primary sensory cortices, such as the impact of leptin in triggering a ‘low power’ mode of  visual cortex function during times of food scarcity (Nathalie Rochefort), and the impact of oxytocin on neuronal function and behaviors related to maternal care, including the integration of auditory signals from pups (Robert Froemke).

All these results highlight the future challenges for defining general principles of contextual modulation of sensory information, and more generally for understanding the multiscale complexity of cortical function. Altogether, the lively discussions during the seminar have been extremely fruitful to identify these challenges and propose novel approaches to address them. These emerging perspectives promise to produce long-lasting and fruitful collaborations among the participants.

 

Criteria used for speaker selection

We used the following criteria to select speakers, in order to ensure the most fruitful discussions and interactions during the meeting. We have ensured a balanced representation in terms of:

  • scientific expertise. We selected investigators tackling the question of sensory information processing at different scales and in different sensory systems:
    • molecular and cellular level, anatomy: Beatriz Rico (visual), Solange Brown (somatosensory)
    • neuronal circuits, functional neurophysiology: Georg Keller (visual), Li Zhang (auditory), Sophie Bagur (auditory), Massimo Scanziani (visual), Mark Andermann (visual), Janelle Pakan (visual, auditory), Pieter Roelfsema (visual), Brice Bathellier (auditory), Jess Cardin (visual), Robert Froemke (auditory), Nathalie Rochefort (visual), Jennifer Bizley (auditory), David Schneider (auditory).
    • computational modeling and machine learning: Jonathan Pillow, Máté Lengyel
  • career stage: 2 junior investigators (Sophie Bagur, post-doctoral researcher and Janelle Pakan, young principal investigator), mid-career principal investigators (Brice Bathellier, Georg Keller, Nathalie Rochefort, Jennifer Bizley, David Schneider, Jess Cardin) and advanced principal investigators (Li Zhang, Massimo Scanziani, Pieter Roelfsema, Robert Froemke, Mark Andermann, Jonathan Pillow, Máté Lengyel, Beatriz Rico, Solange Brown).
  • gender (7 women, 10 men) and geographical origin (9 Europeans and 8 Americans).

OpenEdition vous propose de citer ce billet de la manière suivante :
ldiebold (23 mai 2023). Sensations in action : how behavioural context affects sensory information processing ? / Les sensations en action: comment le contexte comportemental affecte-t-il le traitement de l’information sensorielle? Les carnets de la Fondation des Treilles. Consulté le 14 juillet 2024 à l’adresse https://doi.org/10.58079/qv7s


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