A circuit for navigation in Caenorhabditis elegans

Abstract

Caenorhabditis elegans explores its environment by interrupting its forward movement with occasional turns and reversals. Turns and reversals occur at stable frequencies but irregular intervals, producing probabilistic exploratory behaviors. Here we dissect the roles of individual sensory neurons, interneurons, and motor neurons in exploratory behaviors under different conditions. After animals are removed from bacterial food, they initiate a local search behavior consisting of reversals and deep omega-shaped turns triggered by AWC olfactory neurons, ASK gustatory neurons, and AIB interneurons. Over the following 30 min, the animals disperse as reversals and omega turns are suppressed by ASI gustatory neurons and AIY interneurons. Interneurons and motor neurons downstream of AIB and AIY encode specific aspects of reversal and turn frequency, amplitude, and directionality. SMD motor neurons help encode the steep amplitude of omega turns, RIV motor neurons specify the ventral bias of turns that follow a reversal, and SMB motor neurons set the amplitude of sinusoidal movement. Many of these sensory neurons, interneurons, and motor neurons are also implicated in chemotaxis and thermotaxis. Thus, this circuit may represent a common substrate for multiple navigation behaviors.chemosensation ͉ exploratory behavior ͉ neural circuit A s an animal travels through its environment, its nervous system detects sensory cues, evaluates them based on context and the experience of the animal, and converts this information into adaptive movement. For simple behaviors, sensory neurons sometimes communicate directly with motor neurons, but, in more complex behavioral circuits, several layers of interneurons integrate sensory information and relay it to motor neurons. The path from sensory input to motor output has been defined in only a few cases, including circuits for crustacean feeding (1) and circuits for rapid escape in fish, flies, and nematodes (2-4). In the nematode Caenorhabditis elegans, the escape circuit was defined by using a complete synaptic wiring diagram of the 302 neurons in its nervous system (4, 5). Six mechanosensory neurons that detect noxious stimuli synapse onto four pairs of interneurons called forward and backward command neurons. The command neurons synapse in turn onto motor neurons responsible for forward and backward locomotion, leading to rapid withdrawal from the stimulus. The definition of the escape circuit has enabled analysis of its development, regulation, and modification by experience (6-11). The C. elegans wiring diagram provides an opportunity to define many complete neuronal paths from sensory stimulus to behavior.In contrast with the escape circuit, the neuronal control of locomotion during exploratory behavior is poorly characterized. C. elegans navigates to favorable conditions by chemotaxis, thermotaxis, and aerotaxis. In these sensory behaviors and in exploratory behaviors in the absence of informative sensory cues, the animal moves forward and occasionally changes its direction of move...

Generation and modulation of chemosensory behaviors in C. elegans

“…Shortly upon removal of food, animals exhibit an "arearestricted search behavior" characterized by high frequency of reversals, whereas on prolonged removal of food the frequency of reversals is decreased with coordinated increase in the duration of forward movement [42][43][44][45]. These behaviors are regulated by inputs from distinct sets of chemosensory neurons [42,43].…”

“…It is not yet known whether the synaptic connections between these sensory neurons and interneurons are excitatory or inhibitory. Indeed, the AWC chemosensory neurons are predicted to inhibit the AIY, and activate the AIB interneurons under specific environmental conditions and in response to prior experience, although this remains to be shown physiologically [42][43][44]. Primary interneurons synapse onto a layer of secondary interneurons or motor neurons, which in turn are presynaptic to the command interneurons directing backward or forward locomotory movement [53,66] (Fig.…”

“…A network of additional interneurons and motor neurons direct more subtle but crucial aspects of chemosensory behaviors including the regulation of head and neck movement to allow efficient navigation of chemical gradients [43]. Integration of sensory inputs at these different layers ultimately dictates the duration of time spent by the animal in the forward, as opposed to the backward, moving state, thus regulating movement up or down a chemical gradient (see below) [43,44,64,[66][67][68]. These anatomical and functional mapping studies indicate that in contrast to chemosensory circuits in other model organisms such as Drosophila or the mouse, the chemosensory circuit in C. elegans is relatively shallow.…”

“…As in other chemosensory systems, interaction of an odorant with its cognate ligand is predicted to either activate or inhibit synaptic output of a chemosensory neuron [42,43] (C. Bargmann, personal communication). Although the physiological mechanisms by which activation or inhibition is mediated have not yet been described, many of the molecules required for chemosensory signal transduction have been identified using forward or reverse Fig.…”

Evolution of sustained foraging in three-dimensional environments with physics

“…In biology, despite contributing to the mechanistic explanation of foraging behavior at the genetic [26][27][28][29], molecular [30], and neural levels [31,32], the study of foraging and its evolution has not sufficiently improved our understanding of this phenomenon to the point where it is reproducible in artificial legged animals. One reason for this failure may be that goal-directed behavior in higher animals has taken a very long evolutionary route, by gradually evolving from ancient instances in organisms that can be traced back to the first prokaryotes [30].…”