An ultra-sparse code underlies the generation of neural sequences in a songbird

Sequences of motor activity are encoded in many vertebrate brains by complex spatio-temporal patterns of neural activity; however, the neural circuit mechanisms underlying the generation of these pre-motor patterns are poorly understood. In songbirds, one prominent site of pre-motor activity is the forebrain robust nucleus of the archistriatum (RA), which generates stereotyped sequences of spike bursts during song and recapitulates these sequences during sleep. We show that the stereotyped sequences in RA are driven from nucleus HVC (high vocal centre), the principal pre-motor input to RA. Recordings of identified HVC neurons in sleeping and singing birds show that individual HVC neurons projecting onto RA neurons produce bursts sparsely, at a single, precise time during the RA sequence. These HVC neurons burst sequentially with respect to one another. We suggest that at each time in the RA sequence, the ensemble of active RA neurons is driven by a subpopulation of RA-projecting HVC neurons that is active only at that time. As a population, these HVC neurons may form an explicit representation of time in the sequence. Such a sparse representation, a temporal analogue of the 'grandmother cell' concept for object recognition, eliminates the problem of temporal interference during sequence generation and learning attributed to more distributed representations.     

Neural substrates of vocalization feedback monitoring in primate auditory cortex

Vocal communication involves both speaking and hearing, often taking place concurrently. Vocal production, including human speech and animal vocalization, poses a number of unique challenges for the auditory system. It is important for the auditory system to monitor external sounds continuously from the acoustic environment during speaking despite the potential for sensory masking by self-generated sounds. It is also essential for the auditory system to monitor feedback of one's own voice. This self-monitoring may play a part in distinguishing between self-generated or externally generatedauditory inputs and in detecting errors in our vocal production. Previous work in humans and other animals has demonstrated that the auditory cortex is largely suppressed during speaking or vocalizing. Despite the importance of self-monitoring, the underlying neural mechanisms in the mammalian brain, in particular the role of vocalization-induced suppression, remain virtually unknown. Here we show that neurons in the auditory cortex of marmoset monkeys (Callithrix jacchus) are sensitive to auditory feedback during vocal production, and that changes in the feedback alter the coding properties of these neurons. Furthermore, we found that the previously described cortical suppression during vocalization actually increased the sensitivity of these neurons to vocal feedback. This heightened sensitivity to vocal feedback suggests that these neurons may have an important role in auditory self-monitoring.     

鸣禽鸣啭学习研究进展

禽的鸣啭表现出一种复杂的学习过程，鸣禽学习鸣啭的过程可以分为两个阶段．在感觉学习期，幼鸟必须听到成鸟的鸣啭，并形成鸣啭模板记忆；在感觉运动学习期，鸣禽通过听觉反馈与模板匹配逐步建立稳定的鸣啭．对近年来鸣禽鸣啭学习过程的研究进展进行综述．     

去势对成年雄性斑胸草雀HVC神经元电生理特性的影响

鸣唱控制系统的高级发声中枢HVC（high vocal center）是发声运动通路和前端脑通路的始端，是发声行为的起始控制脑区，亦可接受听觉信号的输入及反馈，是鸣禽鸣唱调控最为重要的脑区.以往研究表明,雄激素及其代谢产物对鸣禽鸣唱控制有重要作用.去势显著改变鸣禽体内激素含量，进而影响鸣禽鸣曲稳定性，但其具体机制尚未阐明.我们运用全细胞膜片钳记录法，在离体细胞水平研究了去势引起的雄激素水平降低对HVC不同神经元电生理特性的影响.研究结果显示,去势组与对照组相比，投射神经元HVCRA，HVCX膜输入电阻减小，膜时间常数降低，动作电位后超极化幅值升高及达到峰值时间延长，表明雄激素可以提高两类投射神经元的兴奋性. 综上所述，雄激素可以一定程度上提高HVC神经元的兴奋性，雄激素可增强HVC对发声运动通路（vocal motor pathway,VMP)的控制，抑制前端脑通路(anterior forebrain pathway,AFP)来实现维持鸣曲的稳定.     

Projection neurons within a vocal motor pathway are born during song learning in zebra finches

Many birds learn song during a restricted 'sensitive' period. Juveniles memorize a song model, and then learn the pattern of muscle contractions necessary to reproduce the song. Of the neural changes accompanying avian song learning, perhaps the most remarkable is the production of new neurons which are inserted into the hyperstriatum ventralis pars caudalis (HVc), a region critical for song production. We report here that in young male zebra finches many of the new neurons incorporated into the HVc innervate the robust nucleus of the archistriatum (RA) which projects to motor neurons controlling the vocal musculature. Furthermore, far fewer of these new neurons are incorporated into the HVc of either adult males that are beyond the sensitive learning period, or young females (who do not develop song). Thus, a major portion of the vocal motor pathway is actually created during song learning. This may enable early sensory experience and vocal practice to not only modify existing neuronal circuits, but also shape the insertion and initial synaptic contacts of neurons controlling adult song.     

Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills

The ability to learn new skills and perfect them with practice applies not only to physical skills but also to abstract skills, like motor planning or neuroprosthetic actions. Although plasticity in corticostriatal circuits has been implicated in learning physical skills, it remains unclear if similar circuits or processes are required for abstract skill learning. Here we use a novel behavioural task in rodents to investigate the role of corticostriatal plasticity in abstract skill learning. Rodents learned to control the pitch of an auditory cursor to reach one of two targets by modulating activity in primary motor cortex irrespective of physical movement. Degradation of the relation between action and outcome, as well as sensory-specific devaluation and omission tests, demonstrate that these learned neuroprosthetic actions are intentional and goal-directed, rather than habitual. Striatal neurons change their activity with learning, with more neurons modulating their activity in relation to target-reaching as learning progresses. Concomitantly, strong relations between the activity of neurons in motor cortex and the striatum emerge. Specific deletion of striatal NMDA receptors impairs the development of this corticostriatal plasticity, and disrupts the ability to learn neuroprosthetic skills. These results suggest that corticostriatal plasticity is necessary for abstract skill learning, and that neuroprosthetic movements capitalize on the neural circuitry involved in natural motor learning.     

鸣禽鸣啭系统的可塑性及长时程增强研究

鸣禽的鸣唱控制系统已成为研究神经系统与学习、行为和发育相关的一个重要模型.鸣禽的鸣啭表现出一种复杂的学习过程.鸣禽学习鸣啭的过程可以分为两个阶段.在感觉学习期,幼鸟必须听到成鸟的鸣啭,并形成鸣啭模板记忆;在感觉运动学习期,鸣禽通过听觉反馈与模板匹配逐步建立稳定的鸣啭.该文对近年来鸣禽鸣啭学习过程中的新生神经元及长时程增强研究进展进行综述.     

Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations

Birdsong, like speech, is a learned vocal behaviour that relies greatly on hearing; in both songbirds and humans the removal of auditory feedback by deafening leads to a gradual deterioration of adult vocal production. Here we investigate the neural mechanisms that contribute to the processing of auditory feedback during the maintenance of song in adult zebra finches. We show that the deleterious effects on song production that normally follow deafening can be prevented by a second insult to the nervous system--the lesion of a basal ganglia-forebrain circuit. The results suggest that the removal of auditory feedback leads to the generation of an instructive signal that actively drives non-adaptive changes in song; they also suggest that this instructive signal is generated within (or conveyed through) the basal ganglia-forebrain pathway. Our findings provide evidence that cortical-basal ganglia circuits may participate in the evaluation of sensory feedback during calibration of motor performance, and demonstrate that damage to such circuits can have little effect on previously learned behaviour while conspicuously disrupting the capacity to adaptively modify that behaviour.     

A possible neuronal basis for Doppler-shift compensation in echo-locating horseshoe bats

The auditory system of the horseshoe bat is finely tuned to the bat's individual vocalization frequency. To compensate for flight-induced Doppler shifts in the echo frequency, the horseshoe bat adjusts the frequency of its echo-location call to maintain the echo frequency within the narrow range to which its auditory system is best tuned. In this report I describe neurons in the midbrain tegmentum of the horseshoe bat, with properties that strongly indicate their involvement in this Doppler-shift compensation. The activity of these neurons was influenced by both sound emission and auditory stimuli. Neuronal discharges in response to vocalization, however, differed from those in response to purely auditory stimuli that mimicked the bat call. When an auditory stimulus was temporally locked to a preceding vocalization, the response was dependent on the time delay between the two. This delay-sensitivity completely disappeared when vocalizations were simulated acoustically. Only those vocalization and 'echo' parameters were encoded that occur in Doppler-shift compensation. In conclusion, I suggest a model for the regulation of the vocalization frequency through auditory feedback.     

Female visual displays affect the development of male song in the cowbird

The role of social stimulation in avian vocal learning is well documented. The separate contribution of social, as opposed to vocal, stimulation has been difficult to address, however, because in almost all cases both tutor and pupil sing. The opportunity to isolate such effects arose in cowbirds (Molothrus ater ater) after discovering that males housed with non-singing female cowbirds made vocal changes which related directly to the female preferences for native song. Here we report how females communicate with males about songs. We describe a visual display by females, a wing stroke, that is elicited by specific vocalizations. The songs that trigger wing strokes are in turn highly effective releasers of copulatory postures, and thus this previously unnoticed female display has biological significance. The data not only provide the first evidence of the tutorial role of male-female interactions during song ontogeny, they also clearly implicate visual stimulation in song learning, a process that has until now been assumed to be affected only by auditory information.     

聋鸟模型的制作

鸟是自然界除人类之外最具复杂发声行为的动物，鸟类语言与人类语言在很多方面都有相似之处，尤其是发声学习的听觉反馈，聋鸟模型的制作可以为其研究鸟类的发声与听觉反馈的关系提供理想的动物模型，本文采用链霉素肌肉注射的方法对鸟进行了致聋试验，结果发现肌肉注射链霉素每日60mg／kg以下为鸟的安全剂量，每日90mg／kg-210mg／kg为鸟的有毒剂量，每日240mg／kg以上为鸟的致死剂量，为聋鸟模型的制作摸索出了一套有效的方法。     

Performance variability enables adaptive plasticity of 'crystallized' adult birdsong

Significant trial-by-trial variation persists even in the most practiced skills. One prevalent view is that such variation is simply 'noise' that the nervous system is unable to control or that remains below threshold for behavioural relevance. An alternative hypothesis is that such variation enables trial-and-error learning, in which the motor system generates variation and differentially retains behaviours that give rise to better outcomes. Here we test the latter possibility for adult bengalese finch song. Adult birdsong is a complex, learned motor skill that is produced in a highly stereotyped fashion from one rendition to the next. Nevertheless, there is subtle trial-by-trial variation even in stable, 'crystallized' adult song. We used a computerized system to monitor small natural variations in the pitch of targeted song elements and deliver real-time auditory disruption to a subset of those variations. Birds rapidly shifted the pitch of their vocalizations in an adaptive fashion to avoid disruption. These vocal changes were precisely restricted to the targeted features of song. Hence, birds were able to learn effectively by associating small variations in their vocal behaviour with differential outcomes. Such a process could help to maintain stable, learned song despite changes to the vocal control system arising from ageing or injury. More generally, our results suggest that residual variability in well learned skills is not entirely noise but rather reflects meaningful motor exploration that can support continuous learning and optimization of performance.     

Brain-wide neuronal dynamics during motor adaptation in zebrafish

A fundamental question in neuroscience is how entire neural circuits generate behaviour and adapt it to changes in sensory feedback. Here we use two-photon calcium imaging to record the activity of large populations of neurons at the cellular level, throughout the brain of larval zebrafish expressing a genetically encoded calcium sensor, while the paralysed animals interact fictively with a virtual environment and rapidly adapt their motor output to changes in visual feedback. We decompose the network dynamics involved in adaptive locomotion into four types of neuronal response properties, and provide anatomical maps of the corresponding sites. A subset of these signals occurred during behavioural adjustments and are candidates for the functional elements that drive motor learning. Lesions to the inferior olive indicate a specific functional role for olivocerebellar circuitry in adaptive locomotion. This study enables the analysis of brain-wide dynamics at single-cell resolution during behaviour.     

Multiple dynamic representations in the motor cortex during sensorimotor learning

The mechanisms linking sensation and action during learning are poorly understood. Layer 2/3 neurons in the motor cortex might participate in sensorimotor integration and learning; they receive input from sensory cortex and excite deep layer neurons, which control movement. Here we imaged activity in the same set of layer 2/3 neurons in the motor cortex over weeks, while mice learned to detect objects with their whiskers and report detection with licking. Spatially intermingled neurons represented sensory (touch) and motor behaviours (whisker movements and licking). With learning, the population-level representation of task-related licking strengthened. In trained mice, population-level representations were redundant and stable, despite dynamism of single-neuron representations. The activity of a subpopulation of neurons was consistent with touch driving licking behaviour. Our results suggest that ensembles of motor cortex neurons couple sensory input to multiple, related motor programs during learning.     

Cross-modal signaling in giant pandas

For solitary species that aggregate to breed, signals, such as sound or odor, transmitted across the landscape can play an important role in mate choice and coordinating breeding activity. Recent work on vocalizations of the giant panda (Ailuropoda melanoleuca), bleats and chirps that are emitted during periods of reproductive activity, has revealed that auditory communication in this species is more complicated and developed than once believed. However, playback experiments using these calls have recorded only a few behaviors over short observation times and the influence of these calls on the signaling behavior of receivers remains unknown. Here, we present results from a pilot study in which we played the bleats of male and female giant pandas in estrus to captive animals and measured vocal and chemical signaling response behavior. We found an increase in scent marking behavior, but not vocalizations, in males and females following the playback of calls made by members of the opposite sex in estrus. To our knowledge, this is the first study to detect a chemical communication response, which was marking, to an auditory signal in giant pandas. Our findings reveal a previously unknown relationship between acoustic and chemical signals in this high profile species and suggest that these two forms of signaling may be interdependent in the social lives of giant pandas.     

Complex auditory behaviour emerges from simple reactive steering

The recognition and localization of sound signals is fundamental to acoustic communication. Complex neural mechanisms are thought to underlie the processing of species-specific sound patterns even in animals with simple auditory pathways. In female crickets, which orient towards the male's calling song, current models propose pattern recognition mechanisms based on the temporal structure of the song. Furthermore, it is thought that localization is achieved by comparing the output of the left and right recognition networks, which then directs the female to the pattern that most closely resembles the species-specific song. Here we show, using a highly sensitive method for measuring the movements of female crickets, that when walking and flying each sound pulse of the communication signal releases a rapid steering response. Thus auditory orientation emerges from reactive motor responses to individual sound pulses. Although the reactive motor responses are not based on the song structure, a pattern recognition process may modulate the gain of the responses on a longer timescale. These findings are relevant to concepts of insect auditory behaviour and to the development of biologically inspired robots performing cricket-like auditory orientation.     

界面核和高级发声中枢与鸣禽鸣曲的学习和维持

鸣禽鸣唱和人类语言都是经过后天学习而获得的。幼鸟在学习鸣唱时先记住教习曲模板，再通过发声反馈比较自鸣曲和模板并调整发声输出，成年后同样需要听觉反馈来维持自鸣曲的特征和稳定。因此，鸣禽听觉系统和运动系统对刺激的感觉运动整合过程是非常重要的。近年研究发现，感觉期幼鸟编码记忆模板的过程需要NIf-HVC投射的参与，同时这一突触联系与维持成年鸣禽可塑性鸣曲空间特征和鸣曲节律至关重要，其中，NMDAR、AchR和NE可能参与调节NIf-HVC突触的效能。HVC类似于人类的Broca区，而NIf类似于人类的Spt区，因此研究NIf-HVC突触在神经环路中的作用有助于揭示人类这两个脑区在语言形成中潜在的功能，有利于探索发声过程相关的感觉运动信息整合的机制     

Neuronal populations and single cells representing learned auditory objects

The neural representations associated with learned auditory behaviours, such as recognizing individuals based on their vocalizations, are not well described. Higher vertebrates learn to recognize complex conspecific vocalizations that comprise sequences of easily identified, naturally occurring auditory objects, which should facilitate the analysis of higher auditory pathways. Here we describe the first example of neurons selective for learned conspecific vocalizations in adult animals--in starlings that have been trained operantly to recognize conspecific songs. The neuronal population is found in a non-primary forebrain auditory region, exhibits increased responses to the set of learned songs compared with novel songs, and shows differential responses to categories of learned songs based on recognition training contingencies. Within the population, many cells respond highly selectively to a subset of specific motifs (acoustic objects) present only in the learned songs. Such neuronal selectivity may contribute to song-recognition behaviour, which in starlings is sensitive to motif identity. In this system, both top-down and bottom-up processes may modify the tuning properties of neurons during recognition learning, giving rise to plastic representations of behaviourally meaningful auditory objects.     

Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song

Cortical-basal ganglia circuits have a critical role in motor control and motor learning. In songbirds, the anterior forebrain pathway (AFP) is a basal ganglia-forebrain circuit required for song learning and adult vocal plasticity but not for production of learned song. Here, we investigate functional contributions of this circuit to the control of song, a complex, learned motor skill. We test the hypothesis that neural activity in the AFP of adult birds can direct moment-by-moment changes in the primary motor areas responsible for generating song. We show that song-triggered microstimulation in the output nucleus of the AFP induces acute and specific changes in learned parameters of song. Moreover, under both natural and experimental conditions, variability in the pattern of AFP activity is associated with variability in song structure. Finally, lesions of the output nucleus of the AFP prevent naturally occurring modulation of song variability. These findings demonstrate a previously unappreciated capacity of the AFP to direct real-time changes in song. More generally, they suggest that frontal cortical and basal ganglia areas may contribute to motor learning by biasing motor output towards desired targets or by introducing stochastic variability required for reinforcement learning.     

Animal behaviour: elephants are capable of vocal learning

There are a few mammalian species that can modify their vocalizations in response to auditory experience--for example, some marine mammals use vocal imitation for reproductive advertisement, as birds sometimes do. Here we describe two examples of vocal imitation by African savannah elephants, Loxodonta africana, a terrestrial mammal that lives in a complex fission-fusion society. Our findings favour a role for vocal imitation that has already been proposed for primates, birds, bats and marine mammals: it is a useful form of acoustic communication that helps to maintain individual-specific bonds within changing social groupings.