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Discriminating external and internal causes for heading changes in freely flying Drosophila.

Censi A, Straw AD, Sayaman RW, Murray RM, Dickinson MH - PLoS Comput. Biol. (2013)

Bottom Line: The remaining turning decisions, not explained by this feature of the visual input, may be attributed to a combination of deterministic processes based on unobservable internal states and purely stochastic behavior.We cannot distinguish these contributions using external observations alone, but we are able to provide a quantitative bound of their relative importance with respect to stimulus-triggered decisions.We discuss how this technique could be generalized for use in other systems and employed as a tool for classifying effects into sensory, decision, and motor categories when used to analyze data from genetic behavioral screens.

View Article: PubMed Central - PubMed

Affiliation: Control & Dynamical Systems, California Institute of Technology, Pasadena, California, United States of America.

ABSTRACT
As animals move through the world in search of resources, they change course in reaction to both external sensory cues and internally-generated programs. Elucidating the functional logic of complex search algorithms is challenging because the observable actions of the animal cannot be unambiguously assigned to externally- or internally-triggered events. We present a technique that addresses this challenge by assessing quantitatively the contribution of external stimuli and internal processes. We apply this technique to the analysis of rapid turns ("saccades") of freely flying Drosophila melanogaster. We show that a single scalar feature computed from the visual stimulus experienced by the animal is sufficient to explain a majority (93%) of the turning decisions. We automatically estimate this scalar value from the observable trajectory, without any assumption regarding the sensory processing. A posteriori, we show that the estimated feature field is consistent with previous results measured in other experimental conditions. The remaining turning decisions, not explained by this feature of the visual input, may be attributed to a combination of deterministic processes based on unobservable internal states and purely stochastic behavior. We cannot distinguish these contributions using external observations alone, but we are able to provide a quantitative bound of their relative importance with respect to stimulus-triggered decisions. Our results suggest that comparatively few saccades in free-flying conditions are a result of an intrinsic spontaneous process, contrary to previous suggestions. We discuss how this technique could be generalized for use in other systems and employed as a tool for classifying effects into sensory, decision, and motor categories when used to analyze data from genetic behavioral screens.

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General reference models for the animal behavior and decision making.Panel A illustrates the nomenclature that we use in this paper:  is the animal configuration (position/velocity), which ultimately depends on the past history of the animal decisions, the body dynamics, and environmental effects, here abstractly represented by the variable . The stimulus  perceived by the animal is a function of the animal configuration  and the geometry/textures of the environment. In the most general terms, the actions of the animals, , are generated on the basis of the instantaneous stimulus  as well as the internal state , which includes, for our purposes, everything which is not observable, including metabolic and neural states. Panel B illustrates the specialization of the model that we postulate. The decisions of the animals are represented by series of observable events belonging to a fixed set of classes; in our case these are left and right body saccades. The events are assumed to be generated by a set of interacting rate-variant Poisson processes. The instantaneous rates  depend on several factors, including the unobservable states, and the external stimulus. The main hypothesis of this paper is that the contribution of the stimulus on the rate can be written as a function of a low-dimensional feature  computed from the stimulus. The inference problem in this paper consists in identifying the functions  that best explain the rates as a function of the stimulus (). The diagram also shows the impact of other unmodeled neural processing based on internal states, acting as a disturbance in the model. We do not infer a functional description of this modeling, but we are able to bound its contribution and show that it is small with respect to the stimulus-induced contribution. The diagram also shows the reduced configuration, the subset of  on which the stimulus actually depends. The reduced configuration depends on the particular experimental settings; in our case, we postulate that in a circular arena the stimulus is dependent on only two degrees of freedom. This is a hypothesis that can be verified a posteriori.
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pcbi-1002891-g002: General reference models for the animal behavior and decision making.Panel A illustrates the nomenclature that we use in this paper: is the animal configuration (position/velocity), which ultimately depends on the past history of the animal decisions, the body dynamics, and environmental effects, here abstractly represented by the variable . The stimulus perceived by the animal is a function of the animal configuration and the geometry/textures of the environment. In the most general terms, the actions of the animals, , are generated on the basis of the instantaneous stimulus as well as the internal state , which includes, for our purposes, everything which is not observable, including metabolic and neural states. Panel B illustrates the specialization of the model that we postulate. The decisions of the animals are represented by series of observable events belonging to a fixed set of classes; in our case these are left and right body saccades. The events are assumed to be generated by a set of interacting rate-variant Poisson processes. The instantaneous rates depend on several factors, including the unobservable states, and the external stimulus. The main hypothesis of this paper is that the contribution of the stimulus on the rate can be written as a function of a low-dimensional feature computed from the stimulus. The inference problem in this paper consists in identifying the functions that best explain the rates as a function of the stimulus (). The diagram also shows the impact of other unmodeled neural processing based on internal states, acting as a disturbance in the model. We do not infer a functional description of this modeling, but we are able to bound its contribution and show that it is small with respect to the stimulus-induced contribution. The diagram also shows the reduced configuration, the subset of on which the stimulus actually depends. The reduced configuration depends on the particular experimental settings; in our case, we postulate that in a circular arena the stimulus is dependent on only two degrees of freedom. This is a hypothesis that can be verified a posteriori.

Mentions: Figure 2A illustrates the conceptual approach of our analysis. We denote by the animal's physical spatial configuration (its position and velocity in a fixed reference frame). The stimulus is the set of all sensory cues perceived by the animal, and it is a function of both the spatial configuration and the appearance of the world . Whereas is a concrete variable that we can possibly measure, the stimulus and the world are placeholders for things that, in general, are unknown. The actions (e.g. saccades in our case) are the external manifestations of the internal neural processing, which depend both on the instantaneous stimulus as well as on , another placeholder variable that represents the animal's internal state (metabolic states, neural states, etc.), and which has dynamics of its own. We assume that it is possible to observe the spatial configuration as well as infer the actions from the observations, but that the internal state is not observable.


Discriminating external and internal causes for heading changes in freely flying Drosophila.

Censi A, Straw AD, Sayaman RW, Murray RM, Dickinson MH - PLoS Comput. Biol. (2013)

General reference models for the animal behavior and decision making.Panel A illustrates the nomenclature that we use in this paper:  is the animal configuration (position/velocity), which ultimately depends on the past history of the animal decisions, the body dynamics, and environmental effects, here abstractly represented by the variable . The stimulus  perceived by the animal is a function of the animal configuration  and the geometry/textures of the environment. In the most general terms, the actions of the animals, , are generated on the basis of the instantaneous stimulus  as well as the internal state , which includes, for our purposes, everything which is not observable, including metabolic and neural states. Panel B illustrates the specialization of the model that we postulate. The decisions of the animals are represented by series of observable events belonging to a fixed set of classes; in our case these are left and right body saccades. The events are assumed to be generated by a set of interacting rate-variant Poisson processes. The instantaneous rates  depend on several factors, including the unobservable states, and the external stimulus. The main hypothesis of this paper is that the contribution of the stimulus on the rate can be written as a function of a low-dimensional feature  computed from the stimulus. The inference problem in this paper consists in identifying the functions  that best explain the rates as a function of the stimulus (). The diagram also shows the impact of other unmodeled neural processing based on internal states, acting as a disturbance in the model. We do not infer a functional description of this modeling, but we are able to bound its contribution and show that it is small with respect to the stimulus-induced contribution. The diagram also shows the reduced configuration, the subset of  on which the stimulus actually depends. The reduced configuration depends on the particular experimental settings; in our case, we postulate that in a circular arena the stimulus is dependent on only two degrees of freedom. This is a hypothesis that can be verified a posteriori.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3585425&req=5

pcbi-1002891-g002: General reference models for the animal behavior and decision making.Panel A illustrates the nomenclature that we use in this paper: is the animal configuration (position/velocity), which ultimately depends on the past history of the animal decisions, the body dynamics, and environmental effects, here abstractly represented by the variable . The stimulus perceived by the animal is a function of the animal configuration and the geometry/textures of the environment. In the most general terms, the actions of the animals, , are generated on the basis of the instantaneous stimulus as well as the internal state , which includes, for our purposes, everything which is not observable, including metabolic and neural states. Panel B illustrates the specialization of the model that we postulate. The decisions of the animals are represented by series of observable events belonging to a fixed set of classes; in our case these are left and right body saccades. The events are assumed to be generated by a set of interacting rate-variant Poisson processes. The instantaneous rates depend on several factors, including the unobservable states, and the external stimulus. The main hypothesis of this paper is that the contribution of the stimulus on the rate can be written as a function of a low-dimensional feature computed from the stimulus. The inference problem in this paper consists in identifying the functions that best explain the rates as a function of the stimulus (). The diagram also shows the impact of other unmodeled neural processing based on internal states, acting as a disturbance in the model. We do not infer a functional description of this modeling, but we are able to bound its contribution and show that it is small with respect to the stimulus-induced contribution. The diagram also shows the reduced configuration, the subset of on which the stimulus actually depends. The reduced configuration depends on the particular experimental settings; in our case, we postulate that in a circular arena the stimulus is dependent on only two degrees of freedom. This is a hypothesis that can be verified a posteriori.
Mentions: Figure 2A illustrates the conceptual approach of our analysis. We denote by the animal's physical spatial configuration (its position and velocity in a fixed reference frame). The stimulus is the set of all sensory cues perceived by the animal, and it is a function of both the spatial configuration and the appearance of the world . Whereas is a concrete variable that we can possibly measure, the stimulus and the world are placeholders for things that, in general, are unknown. The actions (e.g. saccades in our case) are the external manifestations of the internal neural processing, which depend both on the instantaneous stimulus as well as on , another placeholder variable that represents the animal's internal state (metabolic states, neural states, etc.), and which has dynamics of its own. We assume that it is possible to observe the spatial configuration as well as infer the actions from the observations, but that the internal state is not observable.

Bottom Line: The remaining turning decisions, not explained by this feature of the visual input, may be attributed to a combination of deterministic processes based on unobservable internal states and purely stochastic behavior.We cannot distinguish these contributions using external observations alone, but we are able to provide a quantitative bound of their relative importance with respect to stimulus-triggered decisions.We discuss how this technique could be generalized for use in other systems and employed as a tool for classifying effects into sensory, decision, and motor categories when used to analyze data from genetic behavioral screens.

View Article: PubMed Central - PubMed

Affiliation: Control & Dynamical Systems, California Institute of Technology, Pasadena, California, United States of America.

ABSTRACT
As animals move through the world in search of resources, they change course in reaction to both external sensory cues and internally-generated programs. Elucidating the functional logic of complex search algorithms is challenging because the observable actions of the animal cannot be unambiguously assigned to externally- or internally-triggered events. We present a technique that addresses this challenge by assessing quantitatively the contribution of external stimuli and internal processes. We apply this technique to the analysis of rapid turns ("saccades") of freely flying Drosophila melanogaster. We show that a single scalar feature computed from the visual stimulus experienced by the animal is sufficient to explain a majority (93%) of the turning decisions. We automatically estimate this scalar value from the observable trajectory, without any assumption regarding the sensory processing. A posteriori, we show that the estimated feature field is consistent with previous results measured in other experimental conditions. The remaining turning decisions, not explained by this feature of the visual input, may be attributed to a combination of deterministic processes based on unobservable internal states and purely stochastic behavior. We cannot distinguish these contributions using external observations alone, but we are able to provide a quantitative bound of their relative importance with respect to stimulus-triggered decisions. Our results suggest that comparatively few saccades in free-flying conditions are a result of an intrinsic spontaneous process, contrary to previous suggestions. We discuss how this technique could be generalized for use in other systems and employed as a tool for classifying effects into sensory, decision, and motor categories when used to analyze data from genetic behavioral screens.

Show MeSH
Related in: MedlinePlus