Statistical structure of locomotion and its modulation by odors

Liangyu Tao; Siddhi Ozarkar; Jeffrey M Beck; Vikas Bhandawat

doi:10.7554/eLife.41235

Most behaviors such as making tea are not stereotypical but have an obvious structure. However, analytical methods to objectively extract structure from non-stereotyped behaviors are immature. In this study, we analyze the locomotion of fruit flies and show that this non-stereotyped behavior is well-described by a Hierarchical Hidden Markov Model (HHMM). HHMM shows that a fly's locomotion can be decomposed into a few locomotor features, and odors modulate locomotion by altering the time a fly spends performing different locomotor features. Importantly, although all flies in our dataset use the same set of locomotor features, individual flies vary considerably in how often they employ a given locomotor feature, and how this usage is modulated by odor. This variation is so large that the behavior of individual flies is best understood as being grouped into at least three to five distinct clusters, rather than variations around an average fly. Many behaviors that we perform everyday, including something as familiar as making a peanut-butter sandwich, consist of a sequence of recognizable acts. These acts may include, for example, holding a knife and opening a jar. Yet often neither the sequence nor the individual acts are always performed in the exact same way. For example, there are many ways to hold a knife and there are many ways to open a jar, meaning neither of these actions could be called “stereotyped”. A lack of stereotypy makes it difficult for a computer to automatically recognize the individual acts in a sequence. This same problem would apply to other common behaviors, such as walking around somewhere you have not visited before. While we easily recognize it when we see it, walking is not a stereotyped behavior. It consists of a series of movements that differ between individuals, and even in the same individual at different times. So how can someone automatically recognize the individual acts in a non-stereotyped behavior like walking? To begin to find out, Tao et al. developed a mathematical model that can recognize the walking behavior of a fruit fly. Existing recordings of fruit flies walking were analyzed using a type of mathematical model called a Hierarchical Hidden Markov Model (often shortened to HHMM). Such models assume that there are hidden states that influence the behaviors we can see. For example, someone’s chances of going skiing (an observable behavior) depend on whether or not it is winter (a hidden state). The HHMM revealed that the seemingly random wanderings of a fly consist of ten types of movement. These include the “meander”, the “stop-and-walk”, as well as right turns and left turns. Exposing the flies to a pleasant odor – in this case, apple cider vinegar – altered how the flies walked by changing the time they spent performing each of the different types of movement. All flies in the dataset used the same ten movements, but in different proportions. This means that each fly showed an individual pattern of movement. In fact, the differences between flies are so great that Tao et al. argue that there is no such thing as an average walk for a fruit fly. The model represents a complete description of how fruit flies walk. It thus provides clues to the processes that transform an animal’s sensory experiences into behavior. But it also has potential clinical applications. Similar models for human behaviors could help reveal behaviors that are abnormal because of disease. Normal behaviors also show variability, and some diseases increase or decrease this variability. By making it easier to detect these changes, mathematical models could support earlier diagnosis of medical conditions.

Statistical structure of locomotion and its modulation by odors

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Statistical structure of locomotion and its modulation by odors

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