Stable perception of external stimuli over time: oculo-motor and visual processing mechanisms
Lead Research Organisation:
University of Glasgow
Department Name: School of Psychology
Abstract
When the animals populating the floor of the ocean started moving 600 million years ago, they faced an important evolutionary challenge: on one hand self-motion carry clear advantages: for example, finding new sources of food and escaping predators. On the other hand, it introduces ambiguity about the source of a sensory input.
When you are crossing the street, you need to differentiate whether a motion is caused by a movement of a car (that need to be avoided), or a passive movement caused by you crossing the street (which can be ignored).
Any animal that failed to correctly recognize the source of a sensory stimulation would have faced an evolutionary disadvantage, with devastating consequences.
The species that successfully solved this problem did so by keeping track of their movement commands and informing the sensory system about forthcoming movements.
Eye movements are a paradigmatic example of a specific sensory change, induced by the motor system. If we were to perceive the world exactly as it is displayed if front of our eyes, the visual scene would seem a sequence of frequent and large jumps, making any matching attempts between them impossible. It is crucial for the visual system to be able to distinguish 'jumps' that are due to saccades as opposed to changes in the external world. It is believed that the motor system provides the sensory system with a warning of an upcoming movement, to which the central nervous system responds with a compensatory mechanism.
Evidence from monkey neurophysiology shows that several brain locations are particularly involved in the interaction between the oculo-motor system and vision, namely: the frontal and supplementary eye fields in monkey frontal cortex, several portions of the parietal cortex and motion sensitive areas.
We have a general understanding of the fine organizational principles of these areas in monkey neocortex, but the same principles have not been tested in homologue areas of human cortex, so far.
This reflects limitations intrinsic to standard human neuroimaging techniques. The spatial resolution in standard human neuroimaging studies is too coarse to characterize the detailed spatial organization typically observed in monkey neurophysiology. Ultra-high field imaging (7Tesla) helps overcoming these technical limitations, providing better and more detailed signal than standard neuroimaging acquisition. These advantages allow for a more detailed investigation that is not possible to image at lower fields (1.5 and 3Tesla), opening the possibility to test in humans, in vivo, the fine oculomotor-processing principles described in monkey neurophysiology.
When you are crossing the street, you need to differentiate whether a motion is caused by a movement of a car (that need to be avoided), or a passive movement caused by you crossing the street (which can be ignored).
Any animal that failed to correctly recognize the source of a sensory stimulation would have faced an evolutionary disadvantage, with devastating consequences.
The species that successfully solved this problem did so by keeping track of their movement commands and informing the sensory system about forthcoming movements.
Eye movements are a paradigmatic example of a specific sensory change, induced by the motor system. If we were to perceive the world exactly as it is displayed if front of our eyes, the visual scene would seem a sequence of frequent and large jumps, making any matching attempts between them impossible. It is crucial for the visual system to be able to distinguish 'jumps' that are due to saccades as opposed to changes in the external world. It is believed that the motor system provides the sensory system with a warning of an upcoming movement, to which the central nervous system responds with a compensatory mechanism.
Evidence from monkey neurophysiology shows that several brain locations are particularly involved in the interaction between the oculo-motor system and vision, namely: the frontal and supplementary eye fields in monkey frontal cortex, several portions of the parietal cortex and motion sensitive areas.
We have a general understanding of the fine organizational principles of these areas in monkey neocortex, but the same principles have not been tested in homologue areas of human cortex, so far.
This reflects limitations intrinsic to standard human neuroimaging techniques. The spatial resolution in standard human neuroimaging studies is too coarse to characterize the detailed spatial organization typically observed in monkey neurophysiology. Ultra-high field imaging (7Tesla) helps overcoming these technical limitations, providing better and more detailed signal than standard neuroimaging acquisition. These advantages allow for a more detailed investigation that is not possible to image at lower fields (1.5 and 3Tesla), opening the possibility to test in humans, in vivo, the fine oculomotor-processing principles described in monkey neurophysiology.
Technical Summary
The goal of this project is to investigate the human homologue of 3 distinct brain locations involved in oculomotor processing and active vision, building on findings from monkey neurophysiology. I am going to test for the first time whether the fine, within-area organization and computational principles described in monkeys can be observed in humans. I will use a combination of ultra-high field acquisition using functional and structural data. Each brain area will be targeted with a specific experimental design and analysis strategy aimed at characterizing the principles outlined in homologue locations in monkey neocortex.
First, I will test how the oculomotor signal is represented in human neocortex, focusing on human frontal and supplementary eye-fields (FEF/SEF). The laminar and columnar organization of kinematic properties of FEF and SEF in humans is unknown. My goal is to provide a detailed description of this sub-millimeter organization of human FEF and SEF at the structural and functional level.
The parietal lobe will be the focus of the second part. Visual responses from portions of the parietal cortex are modulated by eye position (gain fields). My aim is to identify the locations in parietal cortex where static eye-position is encoded with a gain-field mechanism, providing a first step toward a more comprehensive understanding of the coordinate transformation in human parietal cortex.
Third, I will investigate where and how eye movements are integrated with a dynamic visual input, focusing on the human motion complex. I want to elucidate how the oculomotor signal is implemented, distinguishing between three possibilities: (i) a simple ON-OFF signal, (ii) a scattered representation of the oculomotor signal, (iii) a topographic representation, mapping the kinematics of the movement over the cortex surface.
First, I will test how the oculomotor signal is represented in human neocortex, focusing on human frontal and supplementary eye-fields (FEF/SEF). The laminar and columnar organization of kinematic properties of FEF and SEF in humans is unknown. My goal is to provide a detailed description of this sub-millimeter organization of human FEF and SEF at the structural and functional level.
The parietal lobe will be the focus of the second part. Visual responses from portions of the parietal cortex are modulated by eye position (gain fields). My aim is to identify the locations in parietal cortex where static eye-position is encoded with a gain-field mechanism, providing a first step toward a more comprehensive understanding of the coordinate transformation in human parietal cortex.
Third, I will investigate where and how eye movements are integrated with a dynamic visual input, focusing on the human motion complex. I want to elucidate how the oculomotor signal is implemented, distinguishing between three possibilities: (i) a simple ON-OFF signal, (ii) a scattered representation of the oculomotor signal, (iii) a topographic representation, mapping the kinematics of the movement over the cortex surface.
Planned Impact
The proposed research will act as a bridge between research from monkey neurophysiology and human neuroscience. High-resolution imaging allows researchers to test functional and structural hypotheses in humans, in vivo, at a sub-millimetre scale. The specific hypotheses tested in this proposal are derived from neurophysiology; human neuroimaging and monkey neurophysiology meet in the middle thanks to the high-resolution capabilities of modern ultra-high field imaging. The proposed work will benefit both the field of neuroimaging and neurophysiology, as results from the latter will be tested in vivo, in humans, and data from the former can provide new exiting functional hypotheses for neurophysiology.
Furthermore, the proposed research will increase our understanding of healthy brain functioning, specifically related to eye-movement behaviour and vision.
Several members of staff at the Centre for Cognitive Neuroimaging (CCNi) have established links to imaging-related industries and will benefit from the results and methods developed in this project.
From an economic and societal perspective, the development and implementation of high-resolution (7T) scanners and imaging techniques is one of the recent technological developments that puts into practice the concept of personalized medicine: tailoring treatment for the specific needs of the single patient.
In this regard, recent advances in ultra-high field imaging facilitate non-invasive imaging of the whole brain at an unprecedented level of detail. Standard neuroimaging software is not suited for processing such images and there is a growing need for dedicated tools and analysis strategies that can take ad-vantage of the new data. The analytical approaches used in the proposed projects are thought and im-plemented with the individual participant in mind, characterizing individual idiosyncrasies from the functional and structural perspective, that otherwise would get inevitably lost in the averaging process.
The individual-based approach proposed in this project share the same principles described in individ-ualized medicine and provides the tools to put these principles in practice from a brainimaging perspective.
Benefit from this work will be achieved by publishing and disseminating the work in high impact journals and international conferences as well as news media.
Overall, the fundamental research proposed in this project will contribute to the position of the United Kingdom as a leader in high resolution brain imaging and fundamental research.
Furthermore, the proposed research will increase our understanding of healthy brain functioning, specifically related to eye-movement behaviour and vision.
Several members of staff at the Centre for Cognitive Neuroimaging (CCNi) have established links to imaging-related industries and will benefit from the results and methods developed in this project.
From an economic and societal perspective, the development and implementation of high-resolution (7T) scanners and imaging techniques is one of the recent technological developments that puts into practice the concept of personalized medicine: tailoring treatment for the specific needs of the single patient.
In this regard, recent advances in ultra-high field imaging facilitate non-invasive imaging of the whole brain at an unprecedented level of detail. Standard neuroimaging software is not suited for processing such images and there is a growing need for dedicated tools and analysis strategies that can take ad-vantage of the new data. The analytical approaches used in the proposed projects are thought and im-plemented with the individual participant in mind, characterizing individual idiosyncrasies from the functional and structural perspective, that otherwise would get inevitably lost in the averaging process.
The individual-based approach proposed in this project share the same principles described in individ-ualized medicine and provides the tools to put these principles in practice from a brainimaging perspective.
Benefit from this work will be achieved by publishing and disseminating the work in high impact journals and international conferences as well as news media.
Overall, the fundamental research proposed in this project will contribute to the position of the United Kingdom as a leader in high resolution brain imaging and fundamental research.
People |
ORCID iD |
Alessio Fracasso (Principal Investigator) |
Publications
Battaglia S
(2022)
The Neurobiological Correlates of Gaze Perception in Healthy Individuals and Neurologic Patients.
in Biomedicines
Fracasso A
(2022)
FMRI and intra-cranial electrocorticography recordings in the same human subjects reveals negative BOLD signal coupled with silenced neuronal activity.
in Brain structure & function
Van Dijk JA
(2021)
Validating Linear Systems Analysis for Laminar fMRI: Temporal Additivity for Stimulus Duration Manipulations.
in Brain topography
Almeida J
(2023)
Neural and behavioral signatures of the multidimensionality of manipulable object processing
in Communications Biology
Fabius JH
(2020)
Intra-saccadic displacement sensitivity after a lesion to the posterior parietal cortex.
in Cortex; a journal devoted to the study of the nervous system and behavior
Fabius JH
(2020)
Towards assessing extra-retinal uncertainty: A reply to M. Lisi (2020).
in Cortex; a journal devoted to the study of the nervous system and behavior
Harvey BM
(2020)
A Network of Topographic Maps in Human Association Cortex Hierarchically Transforms Visual Timing-Selective Responses.
in Current biology : CB
Van Dijk JA
(2021)
Laminar processing of numerosity supports a canonical cortical microcircuit in human parietal cortex.
in Current biology : CB
Battaglia S
(2022)
The Influence of Vicarious Fear-Learning in "Infecting" Reactive Action Inhibition.
in Frontiers in behavioral neuroscience
Battaglia S
(2022)
Stopping in (e)motion: Reactive action inhibition when facing valence-independent emotional stimuli.
in Frontiers in behavioral neuroscience
Description | 1) The visual system is composed of several visual space maps located in the posterior part of the brain (the occipital lobe). My team an I improved on some the methods routinely adopted to estimate and visualize these maps and extended the investigation to locations in the frontal and temporal lobes. 2) My team and developed methods to automatically divide macroscopic brain areas into distinguishable components, based on anatomical data. This type of findings is important as relatively large brain areas, previously thought to represent a homogeneous cluster, are shown to be divided into more fundamental components, thus opening the possibility to investigate their specific functions; 3) Vision provides a major source of information for the control of self-movement. It is crucial to be able to distinguish between self motion and movement that occur in the external environement. My team and I developed strategies and methods to study how the visual system integrates active motion (eye movements) with static and dynamic visual input to form a coherent representation of self within the environment. |
Exploitation Route | The primary impact of the proposed project will be to increase our understanding of human oculomotor and visual processing systems with an unprecedented level of detail. The proposed project will act as a bridge between research from monkey neurophysiology and human neuroscience. High-resolution imaging allows researchers to test functional and structural hypotheses in humans, in vivo, at a sub-millimetre scale. The specific hypotheses tested in this proposal are derived from neurophysiology. Human neuroimaging and monkey neurophysiology meet in the middle thanks to the high-resolution capabilities of modern ultra-high field imaging. The proposed work will benefit both the field of neuroimaging and neurophysiology. Results from the latter will be tested in vivo, in humans for the first time, and data from the former can provide new exiting functional hypotheses for neurophysiology. |
Sectors | Digital/Communication/Information Technologies (including Software),Education,Healthcare,Pharmaceuticals and Medical Biotechnology |
URL | https://github.com/AlessioPsych/AnalysisAfni |
Description | Influence on the practice on high-resolution data analysis of MRI/fMRI data |
Geographic Reach | Multiple continents/international |
Policy Influence Type | Membership of a guideline committee |
Description | Eye-movement encoding in human cortex using ultra-high field fMRI (7Tesla) |
Amount | € 45,000 (EUR) |
Funding ID | A-29315 |
Organisation | BIAL Foundation |
Sector | Public |
Country | Portugal |
Start | 02/2022 |
End | 02/2023 |
Description | Modelling content dimension in human neocortex |
Organisation | University of Coimbra |
Country | Portugal |
Sector | Academic/University |
PI Contribution | Between 2021 and 2022 I have established international collaborations with the University of Coimbra (Portugal), with Prof. Jorge Almeida on modelling content dimension in human calcarine and extra calcarine cortex. In this role, I provide knowledge and management for computational methods in MRI as well as theoretical guidance. |
Collaborator Contribution | My partners provided resources and tha manpower to sustain the collaboration |
Impact | 2 manuscripts are currently submitted, and 2 are in preparation. |
Start Year | 2020 |
Description | Myelination in somatosensory cortex across the lifespan |
Organisation | The Otto-von-Guericke University Magdeburg |
Country | Germany |
Sector | Academic/University |
PI Contribution | I am collaborating with Dr. Esther Kuehn (http://www.estherkuehn-science.org/about-me.html) on a project studyin myelination in somatosensory cortex and its variation across the lifespan. |
Collaborator Contribution | I have contributed to the projects providing phd student supervision, code, analysis and pipelines about anatomical segmentation, myelin profile extraction and data analysis. |
Impact | no outcome is available yet. |
Start Year | 2020 |
Description | visuo-motor mapping in epileptic patients, ecog and fMRI |
Organisation | University Medical Center Utrecht (UMC) |
Country | Netherlands |
Sector | Academic/University |
PI Contribution | Provide tools and support for data analysis and processing of fMRI data in a pre-operative setting; Provide information and support for pre-operative mapping of human frontal-eye fields, supplementary eye fields and parietal eye fields; |
Collaborator Contribution | Provide access to the patients in the pre-operative setting; access to fMRI facility, UMC Utrecht access to post-operative ecog facility, UMC Utrecht |
Impact | too early for outcomes |
Start Year | 2019 |