Genetic Dissection of Neural Circuits and Behavior (Advances in Genetics)

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These auxiliary neurons also output to other motor functions, when stimulated alone. Thus, the organization of this circuit allows multiple different types of motor response, as appropriate to the precise nature of the stimulus. A particular challenge in elucidating the mechanisms of mechanosensation has been the identification of the molecules responsible for mechanotransduction.

The existence of readily assayable mechanosensory behaviors, combined with genetic tractability and the ease of cultivating large numbers, makes C. The ability to demonstrate cell-autonomous rescue in the appropriate cell type, and to show a role in mechanically evoked responses in that cell using genetically encoded calcium p. The existence of polymodal neurons such as ASH and PVD opens the door to demonstrating that the role of a protein is mechanosensation specific, as opposed to generally affecting activity of the neuron, whereas heterologous expression can allow demonstration of sufficiency.

As such, they have been instrumental in identifying family members in other species. MEC, on the other hand, is important but not essential for behavioral and calcium responses Chatzigeorgiou et al. When expressed in a heterologous system, neither is sufficient to evoke a mechanosensory response, although MEC-4 d channels do produce constitutively active, amiloride-sensitive currents Goodman et al.

However, coexpression of both in oocytes was recently shown to be sufficient for sheer stress-evoked currents Shi et al.

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The fact that MEC is not essential for gentle touch perhaps suggests that MEC-4 may also trimerize with another, as yet unknown, subunit, also capable of conferring mechanosensitivity. Table 5. Chatzigeorgiou et al. Geffeney et al.

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Han et al. Kang et al. Li et al. Kindt et al. Colbert et al. Sangaletti et al. As Table 5. In addition, however, several diverse transient receptor potential TRP family members are p. TRP-4, for example, appears to play multiple mechanosensory roles in multiple neurons Li et al. The C.

There are at least 38 chemosensory neurons, located mostly at the sensory openings of the amphids and inner labia in the head, and the phasmids in the tail.

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These are ciliated neurons, of diverse morphology; as a general rule, the endings of gustatory neurons are exposed directly to the exterior e. Each expresses a subset of receptors and detects a specific set of attractants, repellants, and pheromones. The ASH nociceptors function in aversion to heavy metals, bitter tastes, and high osmotic strength Hilliard et al.

Distinct neurons are required for attraction versus repulsion. For example, benzaldehyde is sensed by both ASH and AWC; the former functions in repulsion, and the latter in attraction. Thus, the valence of a sensory cue is hardwired into the circuit. This was elegantly demonstrated by heterologous expression of the diacetyl receptor, ODR, which functions in attraction in AWA.

Although the majority of chemosensory neurons appear to be symmetric pairs, expressing the same genes and exhibiting the same functions, there are two intriguing examples of asymmetry, with distinct functional outcomes. In this case, then, asymmetry serves to increase the repertoire of odors that can be distinguished, via activation of characteristic signature combinations of sensory neurons gradients. Interestingly, unlike most bilateral neuron pairs in C.

This raises the possibility that other sensory neurons whose bilateral homologs are not electrically coupled e. ASG might also show lateral asymmetry. An alternative strategy is the integration of sensory input from the amphids in the head and the phasmids in the tail, as seen in the avoidance of the repellent SDS Hilliard et al. ODR, the receptor for diacetyl, for example, was identified in a forward genetic screen for chemotaxis defects, and it was the first GPCR in any organism to be functionally characterized Sengupta et al.

Each chemosensory neuron expresses multiple receptors, in contrast with olfaction in flies and vertebrates, where each olfactory neuron type expresses a single receptor type. Thus, the sensory versatility of each neuron compensates for the small number of sensory neurons. Thermotaxis illustrates the power of the C. AWC also responds to temperature changes, although it is less clear whether this depends on input from other neurons.

Three receptor guanylate cyclases act redundantly to sense temperature in AFD, and they produce cGMP that activates cyclic nucleotide gated channels. Additional genes may also function in thermosensation, potentially as direct temperature sensors.

Genetic Dissection of Neural Circuits: A Decade of Progress

AFD and AWC have both excitatory and inhibitory outputs to the interneuron AIY, and it is the balance between these that determines the precise temperature-correlated activity of AIY and thus thermophilic drive Garrity et al. Interestingly, AFD also functions in detection of noxious heat, using distinct guanylate cyclases, and coupling to distinct downstream circuits, for thermotaxis and thermonociception Liu et al.

For an organism to survive in a changing environment, its nervous system must have the ability to adapt—to balance food finding and reproduction with threat tolerance, and to adjust the balance of the system in this respect, based on experience. Decoding the underlying molecular and circuit mechanisms is extremely challenging, but the relative simplicity of the C.

Despite its relatively small number of neurons, C. When animals are exposed to a high concentration of an attractive cue, in the absence of food starvation, a negative cue , associative learning results, and the attraction is gradually lost over a period of an hour or two. This plasticity is selective for that particular cue, even when several cues are detected by overlapping sensory neurons e. The basic requirement for such a mechanism is that sensory cue and food context are convergently represented to allow association. An emerging theme is that association may occur via a downstream neuromodulatory interneuron, which then acts upon the sensory neuron to change either its dynamic range or its synaptic output.

An example of this Cho et al. The former increases the dynamic range of AWC ON calcium response to butanone, irrespective of pairing with reward or punishment, suggesting that information about odor history is stored in AWC itself. Pairing with food deprivation, on the other hand, requires p.

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A second recent study Ghosh et al. RIM receives inhibitory input from sensory neurons activated by attractive odors e. It in turn provides inhibitory input to forward command neurons and excitatory input to backward command neurons. Animals were surrounded by a high-osmolarity barrier, with a source of diacetyl placed outside it.

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Well-fed animals stay within the barrier, while starvation increases the willingness to ignore the aversive cue to reach the food-indicating attractive odorant. Food deprivation inhibits RIM activity and thus suppresses ASH potentiation, effectively pushing the balance of the circuit in favor of attraction to diacetyl. The 95 rhomboid body wall muscle cells are arranged as staggered paired rows in four quadrants dorsal: left and right; ventral: left and right , each receiving multiple inputs from the 75 motor neurons.

Corresponding muscle cells contract and relax in a reciprocal fashion; for a dorsal bend to occur, for example, the dorsal muscle cells contract while their ventral counterparts relax. For movement to occur, these waveforms must be propagated sequentially to neighboring muscle cells, along the length of the animal, in the appropriate direction; and for movement to be sustained, oscillation between these contracted and relaxed states is required.

Recent advances have helped in the quest to explain how these basic requirements of the motor circuit are achieved for reviews, see Gjorgjieva et al. The D-type neurons are postsynaptic to A- and B-type neurons, and they signal to muscle on the opposing side via inhibitory GABAergic signaling to modulate bending. Proprioceptive cues from anterior or posterior muscle cells also stimulate activity of A- and B-type neurons to drive movement. The ventral nerve cord VNC contains most of the motor neurons that drive undulatory locomotion. The A- and B-type neurons are postsynaptic to five pairs of premotor interneurons, known as the command interneurons.

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The D-type GABAergic neurons are postsynaptic to the A- and B-type neurons and innervate muscle on the opposing side of the body, resulting in contralateral inhibition, although neither the DDs nor VDs are essential for bending Donnelly et al. The cholinergic motor neurons have long neurites devoid of synapses, which, importantly, extend in opposing directions; those of A-type neurons extent anteriorly, while those of B-type neurons extend posteriorly.

During forward movement, when B-type motor neurons sense the bending of more anterior regions, they drive local bending Wen et al. Thus, a bend in a specific location causes a precisely delayed bend at a precise location posterior to this. This simple proprioceptive relationship can explain propagation of the wave in a posterior direction, providing the thrust for forward movement.

Indeed, recent modeling Kunert et al. The opposite orientation of the A-type neurons presumably has the reverse effect, so the direction of movement is determined by whether the A- or B-neurons are exerting control Fig. The decision between forward and backward movement is thus determined by the balance of power between these opposing forces, which in turn depends on the balance of power between the command interneurons, especially AVA and AVB.

The command interneurons are synaptically and electrically interconnected in a complex manner. Although there is no obvious reciprocal wiring to explain how cross inhibition between the forward and reverse command interneurons is achieved, it is clear that this bistable network presents multiple opportunities for intervention by sensory input or neuromodulation. The command interneurons synapse directly onto A- and B-type motor neurons of the ventral nerve cord, and they are also extensively connected to each other.

In this figure, only some of the synaptic connections between the command interneurons are shown. An ambitious project to simultaneously image the activity of a large number of neurons Kato et al. They showed that many p. These states are recurrent and correspond to repeated actions of the worm, providing a common framework on which sensory cues act. This is important, because the state of the network at the time that the stimulus is received will determine how it responds, as Gordus et al. Whereas AWC unfailingly responds to an odor stimulus, the behavioral response is less reliable, and the reason for this lies in the activity state of the circuit.

Their response to the odor stimulus thus depends on their collective activity.

The first genetic screens in C. Although many of these genes affect components of muscle, several unc genes were later found to be critical for the development and function of neurons. These molecules function in axon guidance, the ordered and stereotyped manner of leading axons to their final targets, the processes for which are highly conserved from invertebrates to vertebrates.

The innexins UNC-7 and UNC-9, which, as discussed, are required for gap junction communication between the command interneurons and the cholinergic locomotion motor neurons, were also identified from these genetic screens.

Genetic Dissection of Neural Circuits and Behavior (Advances in Genetics) Genetic Dissection of Neural Circuits and Behavior (Advances in Genetics)
Genetic Dissection of Neural Circuits and Behavior (Advances in Genetics) Genetic Dissection of Neural Circuits and Behavior (Advances in Genetics)
Genetic Dissection of Neural Circuits and Behavior (Advances in Genetics) Genetic Dissection of Neural Circuits and Behavior (Advances in Genetics)
Genetic Dissection of Neural Circuits and Behavior (Advances in Genetics) Genetic Dissection of Neural Circuits and Behavior (Advances in Genetics)
Genetic Dissection of Neural Circuits and Behavior (Advances in Genetics) Genetic Dissection of Neural Circuits and Behavior (Advances in Genetics)

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