Biology subjects

Goldberg, J. H.

Publications and source records attributed to Goldberg, J. H..

14 recordsLinked to original sources

bioRxiv2026

Parrots imitate song and dance with mixed vocal-gestural neural signals

Humans shrug when saying "I don't know" and nod when saying "yes," yet it remains unclear how the brain coordinates vocal and gestural motor systems for learned, multimodal communication. Here we find that budgerigar parrots precisely imitate the fine temporal alignment between song and affiliative headbob gestures. Distinct colonies developed unique vocal-gestural motifs, which reorganized into new shared forms following social re-pairing. Neural recordings from the central nucleus of the anterior arcopallium (AAC), the cortical output of the parrot song system, revealed intermixed representations of vocalizations and head kinematics, including mixed selectivity at the level of single neurons. These findings show that socially learned multimodal communication is implemented by the joint representation of vocal and gestural motor signals within single neurons, revealing neural mechanisms that may extend to frontal cortical regions controlling speech and gesture in humans.

neuroscience↗

bioRxiv2026

A sparse neural code for acoustic targets enables speech-like vocal flexibility in parrots

English speech flexibly recombines 44 phonemes into >20,000 words and limitless phrases. Here we identify a novel neural code supporting combinatorial vocal control in budgerigar parrots. Deep learning based acoustic analyses show that both English imitated and natural warble songs are composed of subsyllabic acoustic elements that are flexibly reused across acoustic contexts, analogous to phoneme reuse in words. Such reuse poses a scaling problem for songbird-inspired timing-based codes, which require distinct neural sequences for distinct syllables even when syllables share acoustic components. We identified neurons in the parrot frontal cortical nucleus MO that exhibit sparse bursts locked to reused acoustic elements independent of syllable identity, timing, or surrounding acoustic context. These results provide the first evidence for a sparse, acoustically-grounded vocal motor code that can be flexibly reused to assemble a large and combinatorial vocal repertoire.

neuroscience↗

bioRxiv2024

A collicular map for touch-guided tongue control

Accurate goal-directed behavior requires the sense of touch to be integrated with information about body position and ongoing motion1,2,3. Behaviors like chewing, swallowing and speech critically depend on precise tactile events on a rapidly moving tongue4,5, but neural circuits for dynamic touch-guided tongue control are unknown. Using high speed videography, we examined 3D lingual kinematics as mice drank from a water spout that unexpectedly changed position during licking, requiring re-aiming in response to subtle contact events on the left, center or right surface of the tongue. Mice integrated information about both precise touch events and tongue position to re-aim ensuing licks. Surprisingly, touch-guided re-aiming was unaffected by photoinactivation of tongue sensory, premotor and motor cortices, but was impaired by photoinactivation of the lateral superior colliculus (latSC). Electrophysiological recordings identified latSC neurons with mechanosensory receptive fields for precise touch events that were anchored in tongue-centered, head-centered or conjunctive reference frames. Notably, latSC neurons also encoded tongue position before contact, information important for tongue-to-head based coordinate transformations underlying accurate touch-guided aiming. Viral tracing revealed tongue sensory inputs to the latSC from the lingual trigeminal nucleus, and optical microstimulation in the latSC revealed a topographic map for aiming licks. These findings demonstrate for the first time that touch-guided tongue control relies on a collicular mechanosensorimotor map, analogous to collicular visuomotor maps associated with visually-guided orienting across many species.

neuroscience↗

bioRxiv2023

Auditory cortical error signals retune during songbird courtship

Auditory feedback is important for vocal learning and control, but it remains unclear how the presence of an audience affects neural representations of self-produced sounds. Here we recorded neural activity from the auditory pallium in zebra finches practicing singing alone and directing courtship songs to females. We first discovered that many auditory neurons changed their singing-related discharge patterns during courtship singing. We used syllable-targeted distorted auditory feedback (DAF) to test how signals related to song feedback distortion depend on courtship context. Though past work showed that dopamine neurons uniformly reduce DAF responses during courtship, pallial auditory neurons exhibited heterogeneous DAF signal re-tuning in the presence of the female. Thus, single neurons in the songbird auditory pallium process feedback from self-produced actions differently when singing alone compared to when singing female-directed courtship song.

neuroscience↗

bioRxiv2023

The songbird lateral habenula projects to dopaminergic midbrain and is important for normal vocal development

Mistakes in performance feel disappointing, suggesting that brain pathways for aversive feedback may play a role in motor learning. Here we tested if the lateral habenula (LHb), an evolutionarily conserved part of the limbic system known in mammals to relay aversive feedback from ventral pallidum (VP) to ventral tegmental area (VTA) dopamine neurons, is involved in birdsong learning and production. By combining viral tract tracing and functional circuit mapping, we discovered that songbird LHb links VP and an auditory cortical area to singing-related DA neurons that signal song errors. As in mammals, VP stimulation activated LHb activity and LHb stimulation suppressed DA firing. To test this pathways role in learning we lesioned the LHb in juvenile zebra finches and recorded their songs in adulthood. Birds with the LHb lesioned as juveniles produced highly unusual vocalizations as adults, including prolonged high-pitch notes and species-atypical trills. These findings identify a songbird VP-LHb-VTA pathway with similar functional connectivity as mammals, expand the known territories of vocal learning circuits, and demonstrate that limbic circuits associated with disappointing outcomes are important for motor performance learning.

neuroscience↗

bioRxiv2023

Songbird mesostriatal dopamine pathways are spatially segregated before the onset of vocal learning

Diverse dopamine (DA) pathways send distinct reinforcement signals to different striatal regions. In adult songbirds, a DA pathway from the ventral tegmental area (VTA) to Area X, the striatal nucleus of the song system, carries singing-related performance error signals important for learning. Meanwhile, a parallel DA pathway to a medial striatal area (MST) arises from a distinct group of neighboring DA neurons that lack connectivity to song circuits and do not encode song error. To test if the structural and functional segregation of these two pathways depends on singing experience, we carried out anatomical studies early in development before the onset of song learning. We find that distinct VTA neurons project to either Area X or MST in juvenile birds before the onset of substantial vocal practice. Quantitative comparisons of early juveniles (30-35 dph), late juveniles (60-65 dph), and adult (>90 dph) brains revealed an outsized expansion in the number of Area X-projecting and MST-projecting VTA neurons over development. These results show that a mesostriatal DA system dedicated to social communication can exist and be spatially segregated before the onset of vocal practice and associated sensorimotor experience.

neuroscience↗

bioRxiv2021

Songbird subthalamic neurons signal song timing and error and project to dopaminergic midbrain

Skill learning requires motor output to be evaluated against internal performance benchmarks. In songbirds, ventral tegmental area (VTA) dopamine neurons (DA) signal performance errors important for learning, but it remains unclear which brain regions project VTA and how these inputs may implement the sensorimotor comparisons necessary for error computation. Here we find that the songbird subthalamic nucleus (STN) projects to VTA and that STN microstimulation can excite VTA neurons. We also discover that STN receives inputs from auditory cortical and ventral pallidal brain regions previously implicated in song evaluation. In the first neural recordings from songbird STN, we discover that the activity of most STN neurons is associated with body movements and not singing, but a small fraction of neurons exhibits precise song timing and performance error signals consistent with performance evaluation. Together our results implicate the STN-VTA projection as an evolutionarily conserved pathway important for motor learning and expand the territories of songbird brain associated with song learning. New & NoteworthySongbird subthalamic (STN) neurons exhibit song-timing and performance error signals and are interconnected with auditory pallium, ventral pallidum and ventral tegmental area, three areas important for song learning.

neuroscience↗

bioRxiv2021

Dopamine Neurons Evaluate Natural Fluctuations in Performance Quality

Many motor skills are learned by comparing ongoing behavior to internal performance benchmarks. Dopamine neurons encode performance error in behavioral paradigms where error is externally induced, but it remains unknown if dopamine also signals the quality of natural performance fluctuations. Here we recorded dopamine neurons in singing birds and examined how spontaneous dopamine spiking activity correlated with natural fluctuations in ongoing song. Antidromically identified basal ganglia-projecting dopamine neurons correlated with recent, and not future, song variations, consistent with a role in evaluation, not production. Furthermore, dopamine spiking was suppressed following the production of outlying vocal variations, consistent with a role for active song maintenance. These data show for the first time that spontaneous dopamine spiking can evaluate natural behavioral fluctuations unperturbed by experimental events such as cues or rewards.

neuroscience↗

bioRxiv2020

Movement signaling in ventral pallidum and dopaminergic midbrain is gated by behavioral state in singing birds

Movement-related neuronal discharge in ventral tegmental area (VTA) and ventral pallidum (VP) is inconsistently observed across studies. One possibility is that some neurons are movement-related and others are not. Another possibility is that the precise behavioral conditions matter - that a single neuron can be movement related under certain behavioral states but not others. We recorded single VTA and VP neurons in birds transitioning between singing and non-singing states, while monitoring body movement with microdrive-mounted accelerometers. Many VP and VTA neurons exhibited body movement-locked activity exclusively when the bird was not singing. During singing, VP and VTA neurons could switch off their tuning to body movement and become instead precisely time-locked to specific song syllables. These changes in neuronal tuning occurred rapidly at state boundaries. Our findings show that movement-related activity in limbic circuits can be gated by behavioral context. Significance statementNeural signals in the limbic system have long been known to represent body movements as well as reward. Here we show that single neurons dramatically change their tuning to movements when a bird starts to sing.

neuroscience↗

bioRxiv2019

Dopamine neurons change their tuning according to courtship context in singing birds

How does courtship affect dopaminergic (DA) responses to reward and motor performance outcomes? We used electrophysiology and fiber photometry to record DA signals in two mesostriatal pathways as thirsty male songbirds sang alone and to females. When alone, water reward signals were observed globally but singing-related performance error signals were restricted to a song-specialized mesostriatal pathway. During courtship singing, DA responses to both water-predicting cues and song performance outcomes diminished, and DA signals in the song pathway were instead driven by female calls timed with the male song. Thus DA signals are dynamically gated and routed through distinct pathways as animals change their priorities in response to a courtship opportunity.

neuroscience↗

bioRxiv2019

Tongue Kinematics. Cortex-dependent corrections as the mouse tongue reaches for, and misses, targets

AbstractPrecise tongue control is necessary for drinking, eating, and vocalizing1, 2. Yet because tongue movements are fast and difficult to resolve, neural control of lingual kinematics remains poorly understood. Here we combine kilohertz frame-rate imaging and a deep learning based neural network to resolve 3D tongue kinematics in mice drinking from a water spout. Successful licks required previously unobserved corrective submovements (CSMs) which, like online corrections during primate reaches3-10, occurred after the tongue missed unseen, distant, or displaced targets. Photoinhibition of anterolateral motor cortex (ALM) impaired online corrections, resulting in hypometric licks that missed the spout. ALM neural activity reflected upcoming, ongoing, and past CSMs, as well as errors in predicted spout contact. Though less than a tenth of a second in duration, a single mouse lick exhibits hallmarks of online motor control associated with a primate reach, including cortex-dependent corrections after misses.

neuroscience↗

bioRxiv2018

A circuit motif in the songbird basal ganglia for computing predicted performance quality

Ventral tegmental area (VTA) dopamine neurons signal prediction error, the difference between actual and predicted outcome, but it remains unclear how error is computed. Here we identify in songbirds a ventral basal ganglia (vBG) region that is required for song learning and that sends prediction error signals to VTA. During singing, vBG neurons heterogeneously encoded song timing, auditory error, predicted error, and the difference between the two (prediction error). Viral tracing revealed inputs to vBG from auditory and vocal motor thalamus, auditory and vocal motor cortex, and VTA. Our findings reveal a classic actor-critic circuit motif in which a ventral critic learns the prediction component of a prediction error signal that is relayed by VTA to a dorsal actor (the vocal motor BG nucleus Area X). A circuit motif for computing reward prediction error can compute predicted performance quality during motor sequence learning.

neuroscience↗

bioRxiv2018

Cortical control of kinematic primitives in mice performing a hold-still-center-out reach task

Motor sequences are constructed from primitives, hypothesized building blocks of movement, but mechanisms of primitive generation remain unclear. Using automated homecage training and a novel forelimb sensor, we trained freely-moving mice to initiate forelimb sequences with clearly resolved submillimeter-scale micromovements followed by millimeter-scale reaches to learned spatial targets. Hundreds of thousands of trajectories were decomposed into millions of kinematic primitives, while closed-loop photoinhibition was used to test roles of motor cortical areas. Inactivation of contralateral motor cortex reduced primitive peak speed but, surprisingly, did not substantially affect primitive direction, initiation, termination, or complexity, resulting in isomorphic, spatially contracted trajectories that undershot targets. Our findings demonstrate separable loss of a single kinematic parameter, speed, and identify conditions where loss of cortical drive reduces the gain of motor primitives but does not affect their generation, timing or direction. The combination of high precision forelimb sensing with automated training and neural manipulation provides a system for studying how motor sequences are constructed from elemental building blocks.

neuroscience↗

bioRxiv2017

The segregation of vocal circuits solves a credit assignment problem associated with multi-objective reinforcement learning

Motor circuits vary in topographic organization, ranging from a coarse relationship between neuron location and function to highly localized regions controlling specific behaviors. For unclear reasons, vocal learning circuits lie at this second extreme: they repeatedly evolved to be spatially segregated from other parts of the motor system. Here we show that spatially segregated motor circuits can solve a specific problem that arises when an animal tries to learn two things at once. We trained songbirds in vocal and place learning paradigms with brief strobe light flashes and noise bursts. Strobe light negatively reinforced place learning but did not affect song syllable learning. Noise bursts positively reinforced place preference but negatively reinforced syllable learning. These double dissociations indicate that vocalization-related reinforcement signals specifically target the vocal motor system, while place-related reinforcement signals specifically target the navigation system. Non-global, target-specific reinforcement signals have established utility in machine implementation of multi-objective learning. In vocal learners, such signals could enable an animal to practice vocalizing as it does other things such as forage for food or learn to walk.

neuroscience↗