Cholinergic Sensorimotor Integration Regulates Olfactory Steering.

December 21, 2017

Liu H, Yang W, Wu T, Duan F, Soucy E, Jin X, Zhang Y

Sensorimotor integration regulates goal-directed movements. We study the signaling mechanisms underlying sensorimotor integration in C. elegans during olfactory steering, when the sinusoidal movements of the worm generate an in-phase oscillation in the concentration of the sampled odorant. We show that cholinergic neurotransmission encodes the oscillatory sensory response and the motor state of head undulations by acting through an acetylcholine-gated channel and a muscarinic acetylcholine receptor, respectively. These signals converge on two axonal domains of an interneuron RIA, where the sensory-evoked signal suppresses the motor-encoding signal to transform the spatial information of the odorant into the asymmetry between the axonal activities. The asymmetric synaptic outputs of the RIA axonal domains generate a directional bias in the locomotory trajectory. Experience alters the sensorimotor integration to generate specific behavioral changes. Our study reveals how cholinergic neurotransmission, which can represent sensory and motor information in the mammalian brain, regulates sensorimotor integration during goal-directed locomotions.


Development of self-protective biases in response to social evaluative feedback.

November 27, 2017

Rodman AM, Powers KE, Somerville LH

Adolescence is a developmental period marked by heightened attunement to social evaluation. While adults have been shown to enact self-protective processes to buffer their self-views from evaluative threats like peer rejection, it is unclear whether adolescents avail themselves of the same defenses. The present study examines how social evaluation shapes views of the self and others differently across development. N = 107 participants ages 10-23 completed a reciprocal social evaluation task that involved predicting and receiving peer acceptance and rejection feedback, along with assessments of self-views and likability ratings of peers. Here, we show that, despite equivalent experiences of social evaluation, adolescents internalized peer rejection, experiencing a feedback-induced drop in self-views, whereas adults externalized peer rejection, reporting a task-induced boost in self-views and deprecating the peers who rejected them. The results identify codeveloping processes underlying why peer rejection may lead to more dramatic alterations in self-views during adolescence than other phases of the lifespan.

Ten-month-old infants infer the value of goals from the costs of actions.

November 24, 2017

Liu S, Ullman TD, Tenenbaum JB, Spelke ES

Infants understand that people pursue goals, but how do they learn which goals people prefer? We tested whether infants solve this problem by inverting a mental model of action planning, trading off the costs of acting against the rewards actions bring. After seeing an agent attain two goals equally often at varying costs, infants expected the agent to prefer the goal it attained through costlier actions. These expectations held across three experiments that conveyed cost through different physical path features (height, width, and incline angle), suggesting that an abstract variable-such as "force," "work," or "effort"-supported infants' inferences. We modeled infants' expectations as Bayesian inferences over utility-theoretic calculations, providing a bridge to recent quantitative accounts of action understanding in older children and adults.


Evolution and Genetics of Precocious Burrowing Behavior in Peromyscus Mice.

November 23, 2017

Metz HC, Bedford NL, Pan YL, Hoekstra HE

A central challenge in biology is to understand how innate behaviors evolve between closely related species. One way to elucidate how differences arise is to compare the development of behavior in species with distinct adult traits [1]. Here, we report that Peromyscus polionotus is strikingly precocious with regard to burrowing behavior, but not other behaviors, compared to its sister species P. maniculatus. In P. polionotus, burrows were excavated as early as 17 days of age, whereas P. maniculatus did not build burrows until 10 days later. Moreover, the well-known differences in burrow architecture between adults of these species-P. polionotus adults excavate long burrows with an escape tunnel, whereas P. maniculatus dig short, single-tunnel burrows [2-4]-were intact in juvenile burrowers. To test whether this juvenile behavior is influenced by early-life environment, we reciprocally cross-fostered pups of both species. Fostering did not alter the characteristic burrowing behavior of either species, suggesting that these differences are genetic. In backcross hybrids, we show that precocious burrowing and adult tunnel length are genetically correlated and that a P. polionotus allele linked to tunnel length variation in adults is also associated with precocious onset of burrowing in juveniles, suggesting that the same genetic region-either a single gene with pleiotropic effects or linked genes-influences distinct aspects of the same behavior at these two life stages. These results raise the possibility that genetic variants affect behavioral drive (i.e., motivation) to burrow and thereby affect both the developmental timing and adult expression of burrowing behavior.

Curr. Biol.

Gaze-Stabilizing Central Vestibular Neurons Project Asymmetrically to Extraocular Motoneuron Pools.

November 22, 2017

Schoppik D, Bianco IH, Prober DA, Douglass AD, Robson DN, Li JMB, Greenwood JSF, Soucy E, Engert F, Schier AF

Within reflex circuits, specific anatomical projections allow central neurons to relay sensations to effectors that generate movements. A major challenge is to relate anatomical features of central neural populations, such as asymmetric connectivity, to the computations the populations perform. To address this problem, we mapped the anatomy, modeled the function, and discovered a new behavioral role for a genetically defined population of central vestibular neurons in rhombomeres 5-7 of larval zebrafish. First, we found that neurons within this central population project preferentially to motoneurons that move the eyes downward. Concordantly, when the entire population of asymmetrically projecting neurons was stimulated collectively, only downward eye rotations were observed, demonstrating a functional correlate of the anatomical bias. When these neurons are ablated, fish failed to rotate their eyes following either nose-up or nose-down body tilts. This asymmetrically projecting central population thus participates in both upward and downward gaze stabilization. In addition to projecting to motoneurons, central vestibular neurons also receive direct sensory input from peripheral afferents. To infer whether asymmetric projections can facilitate sensory encoding or motor output, we modeled differentially projecting sets of central vestibular neurons. Whereas motor command strength was independent of projection allocation, asymmetric projections enabled more accurate representation of nose-up stimuli. The model shows how asymmetric connectivity could enhance the representation of imbalance during nose-up postures while preserving gaze stabilization performance. Finally, we found that central vestibular neurons were necessary for a vital behavior requiring maintenance of a nose-up posture: swim bladder inflation. These observations suggest that asymmetric connectivity in the vestibular system facilitates representation of ethologically relevant stimuli without compromising reflexive behavior.

SIGNIFICANCE STATEMENT Interneuron populations use specific anatomical projections to transform sensations into reflexive actions. Here we examined how the anatomical composition of a genetically defined population of balance interneurons in the larval zebrafish relates to the computations it performs. First, we found that the population of interneurons that stabilize gaze preferentially project to motoneurons that move the eyes downward. Next, we discovered through modeling that such projection patterns can enhance the encoding of nose-up sensations without compromising gaze stabilization. Finally, we found that loss of these interneurons impairs a vital behavior, swim bladder inflation, that relies on maintaining a nose-up posture. These observations suggest that anatomical specialization permits neural circuits to represent relevant features of the environment without compromising behavior.