In songbirds, the basal ganglia outflow nucleus LMAN is a cortical analog that is required for several forms of song plasticity and learning. Moreover, in adults, inactivating LMAN can reverse the initial expression of learning driven via aversive reinforcement. In the present study, we investigated how LMAN contributes to both reinforcement-driven learning and a self-driven recovery process in adult Bengalese finches. We first drove changes in the fundamental frequency of targeted song syllables and compared the effects of inactivating LMAN with the effects of interfering with N-methyl-d-aspartate (NMDA) receptor-dependent transmission from LMAN to one of its principal targets, the song premotor nucleus RA. Inactivating LMAN and blocking NMDA receptors in RA caused indistinguishable reversions in the expression of learning, indicating that LMAN contributes to learning through NMDA receptor-mediated glutamatergic transmission to RA. We next assessed how LMAN's role evolves over time by maintaining learned changes to song while periodically inactivating LMAN. The expression of learning consolidated to become LMAN independent over multiple days, indicating that this form of consolidation is not completed over one night, as previously suggested, and instead may occur gradually during singing. Subsequent cessation of reinforcement was followed by a gradual self-driven recovery of original song structure, indicating that consolidation does not correspond with the lasting retention of changes to song. Finally, for self-driven recovery, as for reinforcement-driven learning, LMAN was required for the expression of initial, but not later, changes to song. Our results indicate that NMDA receptor-dependent transmission from LMAN to RA plays an essential role in the initial expression of two distinct forms of vocal learning and that this role gradually wanes over a multiday process of consolidation. The results support an emerging view that cortical-basal ganglia circuits can direct the initial expression of learning via top-down influences on primary motor circuitry.

Despite their small brains, insects can navigate over long distances by orienting using visual landmarks [1], skylight polarization [2-9], and sun position [3, 4, 6, 10]. Although Drosophila are not generally renowned for their navigational abilities, mark-and-recapture experiments in Death Valley revealed that they can fly nearly 15 km in a single evening [11]. To accomplish such feats on available energy reserves [12], flies would have to maintain relatively straight headings, relying on celestial cues [13]. Cues such as sun position and polarized light are likely integrated throughout the sensory-motor pathway [14], including the highly conserved central complex [4, 15, 16]. Recently, a group of Drosophila central complex cells (E-PG neurons) have been shown to function as an internal compass [17-19], similar to mammalian head-direction cells [20]. Using an array of genetic tools, we set out to test whether flies can navigate using the sun and to identify the role of E-PG cells in this behavior. Using a flight simulator, we found that Drosophila adopt arbitrary headings with respect to a simulated sun, thus performing menotaxis, and individuals remember their heading preference between successive flights-even over several hours. Imaging experiments performed on flying animals revealed that the E-PG cells track sun stimulus motion. When these neurons are silenced, flies no longer adopt and maintain arbitrary headings relative to the sun stimulus but instead exhibit frontal phototaxis. Thus, without the compass system, flies lose the ability to execute menotaxis and revert to a simpler, reflexive behavior.

No abstract

Reinforcement signals indicating success or failure are known to alter the probability of selecting between distinct actions. However, successful performance of many motor skills, such as speech articulation, also requires learning behavioral trajectories that vary continuously over time. Here, we investigated how temporally discrete reinforcement signals shape a continuous behavioral trajectory, the fundamental frequency of adult Bengalese finch song. We provided reinforcement contingent on fundamental frequency performance only at one point in song. Learned changes to fundamental frequency were maximal at this point, but also extended both earlier and later in the fundamental frequency trajectory. A simple principle predicted the detailed structure of learning; birds learn to produce the average of the behavioral trajectories associated with successful outcomes. This learning rule accurately predicts the structure of learning at a millisecond time scale, demonstrating that the nervous system records fine-grained details of successful behavior and uses this information to guide learning.

Animals must use external cues to maintain a straight course over long distances. In this study, we investigated how the fruit fly selects and maintains a flight heading relative to the axis of linearly polarized light, a visual cue produced by the atmospheric scattering of sunlight. To track flies' headings over extended periods, we used a flight simulator that coupled the angular velocity of dorsally presented polarized light to the stroke amplitude difference of the animals' wings. In the simulator, most flies actively maintained a stable heading relative to the axis of polarized light for the duration of 15 min flights. We found that individuals selected arbitrary, unpredictable headings relative to the polarization axis, which demonstrates that can perform proportional navigation using a polarized light pattern. When flies flew in two consecutive bouts separated by a 5 min gap, the two flight headings were correlated, suggesting individuals retain a memory of their chosen heading. We found that adding a polarized light pattern to a light intensity gradient enhanced flies' orientation ability, suggesting use a combination of cues to navigate. For both polarized light and intensity cues, flies' capacity to maintain a stable heading gradually increased over several minutes from the onset of flight. Our findings are consistent with a model in which each individual initially orients haphazardly but then settles on a heading which is maintained via a self-reinforcing process. This may be a general dispersal strategy for animals with no target destination.

To follow a straight course, animals must maintain a constant heading relative to a fixed, distant landmark, a strategy termed menotaxis. In experiments using a flight simulator, we found that Drosophila adopt arbitrary headings with respect to a simulated sun, and individuals remember their heading preference between successive flights—even over gaps lasting several hours. Imaging experiments revealed that a class of neurons within the central complex, which have been previously shown to act as an internal compass, track the azimuthal motion of a sun stimulus. When these neurons are silenced, flies no longer adopt and maintain arbitrary headings, but instead exhibit frontal phototaxis. Thus, without the compass system, flies lose the ability to execute menotaxis and revert to a simpler, reflexive behavior.One sentence summarySilencing the compass neurons in the central complex of Drosophila eliminates sun navigation but leaves phototaxis intact.

Variation in sequencing of actions occurs in many natural behaviors, yet how such variation is maintained is poorly understood. We investigated maintenance of sequence variation in adult Bengalese finch song, a learned skill with rendition-to-rendition variation in the sequencing of discrete syllables (i.e., syllable "b" might transition to "c" with 70% probability and to "d" with 30% probability). We found that probabilities of transitions ordinarily remain stable but could be modified by delivering aversive noise bursts following one transition (e.g., "b3c") but not the alternative (e.g., "b3d"). Such differential reinforcement induced gradual, adaptive decreases in probabilities of targeted transitions and compensatory increases in alternative transitions. Thus, the normal stability of transition probabilities does not reflect hardwired premotor circuitry. While all variable transitions could be modified by differential reinforcement, some were less readily modified than others; these were cases that exhibited more alternation between possible transitions than predicted by chance (i.e., "b3d " would tend to follow "b3c " and vice versa). These history-dependent transitions were less modifiable than more stochastic transitions. Similarly, highly stereotyped transitions (which are completely predictable) were not modifiable. This suggests that stochastically generated variability is crucial for sequence modification. Finally, we found that, when reinforcement ceased, birds gradually restored transition probabilities to their baseline values. Hence, the nervous system retains a representation of baseline probabilities and has the impetus to restore them. Together, our results indicate that variable sequencing in a motor skill can reflect an end point of learning that is stably maintained via continual self-monitoring.

Many casual observers typecast Drosophila melanogaster as a stationary pest that lurks around fruit and wine. However, the omnipresent fruit fly, which thrives even in desert habitats, likely established and maintained its cosmopolitan status via migration over large spatial scales. To perform long-distance dispersal, flies must actively maintain a straight compass heading through the use of external orientation cues, such as those derived from the sky. In this Review, we address how D. melanogaster accomplishes longdistance navigation using celestial cues. We focus on behavioral and physiological studies indicating that fruit flies can navigate both to a pattern of linearly polarized light and to the position of the sunthe same cues utilized by more heralded insect navigators such as monarch butterflies and desert ants. In both cases, fruit flies perform menotaxis, selecting seemingly arbitrary headings that they then maintain over time. We discuss how the fly's nervous system detects and processes this sensory information to direct the steering maneuvers that underlie navigation. In particular, we highlight recent findings that compass neurons in the central complex, a set of midline neuropils, are essential for navigation. Taken together, these results suggest that fruit flies share an ancient, latent capacity for celestial navigation with other insects. Furthermore, they illustrate the potential of D. melanogaster to help us to elucidate both the cellular basis of navigation and mechanisms of directed dispersal on a landscape scale.