The space of actions - Neural circuits for transforming spatial representations into actions
Lead Research Organisation:
MRC LABORATORY OF MOLECULAR BIOLOGY
Department Name: Neurobiology
Abstract
I hear a familiar voice and I turn towards its source, I see a car approaching and I move away from it, I smell a cup of coffee and I reach for it. All these daily experiences are ultimately linked to our innate sense of space, we know where things around us are and how to interact with them. In other words, we are able to bind multisensory experiences into a coherent percept and allocate it in a meaningful spatial frame so to appropriately direct our actions. But how this multisensory binding occurs, how such a coherent mental spatial frame is constructed and how it is finally implemented to direct actions remain largely unresolved questions.
In recent years, we have begun to understand how animals encode spatial information in the form of allocentric maps, in the context of navigation. Similarly, spatially tuned actions such as reaching and orienting may rely on an egocentric map of peripersonal space, whose neural implementation becomes overt in the motor domain with the production of appropriate movement vectors. In comparison with navigational space, the neural basis of the encoding of peripersonal space ("the space within reach") as well as the neural mechanisms for its implementation into actions remain far less characterised. In this proposal I will assess the overarching hypothesis that this representation is routed in the motor domain and depends on motor execution. I hypothesise that brains construct cognitive and perceptual spatial representations by relying on the activity of networks involved in the planning and the control of three-dimensional bodily movements. In the words of Henry Poincaré, the French mathematician, "localising an object means representing to ourselves the movements that must take place to reach that object". Thus, in line with recent efforts to study perceptual and cognitive abilities as enactive processes (i.e. processes whose primary goal is to guide action), I propose and aim to test a kinetic, motor-routed theory of spatial cognition. I will argue that the most fruitful path to this goal is to start from the motor end of the problem, i.e. from the neuronal populations responsible for the generation of spatially tuned movements, and progressively move upstream to unravel circuits and computations responsible for their planning, selection and control.
In recent years, we have begun to understand how animals encode spatial information in the form of allocentric maps, in the context of navigation. Similarly, spatially tuned actions such as reaching and orienting may rely on an egocentric map of peripersonal space, whose neural implementation becomes overt in the motor domain with the production of appropriate movement vectors. In comparison with navigational space, the neural basis of the encoding of peripersonal space ("the space within reach") as well as the neural mechanisms for its implementation into actions remain far less characterised. In this proposal I will assess the overarching hypothesis that this representation is routed in the motor domain and depends on motor execution. I hypothesise that brains construct cognitive and perceptual spatial representations by relying on the activity of networks involved in the planning and the control of three-dimensional bodily movements. In the words of Henry Poincaré, the French mathematician, "localising an object means representing to ourselves the movements that must take place to reach that object". Thus, in line with recent efforts to study perceptual and cognitive abilities as enactive processes (i.e. processes whose primary goal is to guide action), I propose and aim to test a kinetic, motor-routed theory of spatial cognition. I will argue that the most fruitful path to this goal is to start from the motor end of the problem, i.e. from the neuronal populations responsible for the generation of spatially tuned movements, and progressively move upstream to unravel circuits and computations responsible for their planning, selection and control.
People |
ORCID iD |
| Marco Tripodi (Principal Investigator) |
Publications
Ciabatti E
(2023)
Genomic stability of self-inactivating rabies.
in eLife
González-Rueda A
(2024)
Kinetic features dictate sensorimotor alignment in the superior colliculus.
in Nature
Lee H
(2023)
Combining long-term circuit mapping and network transcriptomics with SiR-N2c.
in Nature methods
| Description | 1. Translating visual information into motor commands is essential for our everyday interactions with the world, enabling us to convert sensory input into appropriate motor responses. While extensive research has characterized the circuits responsible for sensory representation and motor output generation, the circuitry bridging sensation and action has remained elusive. Our recent has shed light onto this mystery by identifying the neural mechanisms underpinning visuomotor transformations. Recent findings have shown that two visual pathways coexist within the superior colliculus. One pathway is dedicated to responding to static visual features, with each point in the visual scene topographically mapped onto the surface of the superior colliculus. The other pathway, whose existence only recently emerged, is instead dedicated to responding to moving visual stimuli. This second pathway is also topographically organized so that neurons responding to the same orientation of motion cluster together, forming coherent motion direction columns. The conventional textbook model of sensorimotor alignment always assumed that the static visual pathway drove the motor areas. Contrary to this model, these new findings reveal that the motor system is driven instead by the neurons forming the newly discovered motion direction columns. Essentially, the system functions like a motion detection camera, which activates in the presence of moving objects and reports to the motor system both the location and direction of the object, thus facilitating its rapid interception through the recruitment of movement vectors that are aligned to the target trajectory but opposite in direction. Importantly, previous work in the Tripodi lab has revealed that the collicular motor system is also topographically organized so that neurons driving motion in the same direction cluster together, forming discrete and direction-coherent motor columns. These new findings indicate that sensorimotor alignment is achieved by simply aligning these two modular direction systems, so that visual direction columns are connected to motor direction columns of the same orientation but opposite direction. 2. We have optimized a new non-toxic viral delivery system able to target the central nervous system that has minimal impact on cellular physiology and can hence be used to deliver therapeutic agents. |
| Exploitation Route | 1. From a basic science discovery perspective, this new discovery encourages a profound rethinking of the logic of sensory representation in the context of action control, suggesting that other sensory modalities might be represented in a similar modular fashion and according to the same kinetic criteria. For example, in the context of sensorimotor integration, one might expect that the most useful representation of auditory space would be that of directional sound sweeps, and that similar direction columns for sound might also exist. From a a more applied engineering perspective, the work might stimulate a rethinking about how we should train robotic systems in order for them to learn to interact with the environment. 2. The future of the technology, beyond its application in basic science, is to deliver therapeutic agents in the context of neurodegenerative conditions. |
| Sectors | Education Healthcare Pharmaceuticals and Medical Biotechnology |
| URL | https://www.nature.com/articles/s41592-023-01803-4 |
| Description | The findings of our work on engineered non-toxic viruses have been incorporated into a patent for the development of a novel system designed to deliver therapeutic agents to the nervous system. The long-term goal is to utilize this system for the targeted delivery of therapeutic agents in the treatment of neurodegenerative diseases. |
| First Year Of Impact | 2024 |
| Sector | Pharmaceuticals and Medical Biotechnology |