The structure and connectivity of the forebrain nucleus HVc, a site of sensorimotor integration in the song control system of oscine birds, were investigated in adult zebra finches. HVc in males comprises three cytoarchitectonic subdivisions: the commonly recognized central region with large and medium-sized darkly staining cells, a ventral caudomedial region with densely packed small and medium-sized cells, and a dorsolateral region with oblong cells and rows of cells. All three subdivisions project to area X and the robust nucleus of the archistriatum, with more complexity in the classes and distribution of cells than previously reported. In females, HVc is very small and has a cytoarchitecture distinct from that of the three male subdivisions. The structure of HVc in females treated with estradiol at 15 days of age is similar to male HVc. Tracer studies in males with fluorescent and biotinylated dextrans demonstrate non-topographic projections onto HVc that may carry auditory information, including type 1 and type 2 neurons in subdivisions L1 and L3 of the field L complex, a class of neurons in nucleus interface, nucleus uvaeformis, the caudal neostriatum ventral to HVc, and intrinsic HVc connections. These data are interpreted in terms of HVc's functional properties. Additionally, the neostriatum immediately ventral to HVc receives projections from field L, ventral hyperstriatum, and caudal neostriatum, and projects to a region surrounding RA and near to or into area X. The similarity of the connectivity of HVc and adjacent neostriatum suggests the possibility that they share a common origin.
How do neural systems process sensory information to control locomotion? The weakly electric knifefish Eigenmannia, an ideal model for studying sensorimotor control, swims to stabilize the sensory image of a sinusoidally moving refuge. Tracking performance is best at stimulus frequencies less than ϳ1 Hz. Kinematic analysis, which is widely used in the study of neural control of movement, predicts commensurately low-pass sensory processing for control. The inclusion of Newtonian mechanics in the analysis of the behavior, however, categorically shifts the prediction: this analysis predicts that sensory processing is high pass. The counterintuitive prediction that a low-pass behavior is controlled by a high-pass neural filter nevertheless matches previously reported but poorly understood high-pass filtering seen in electrosensory afferents and downstream neurons. Furthermore, a model incorporating the high-pass controller matches animal behavior, whereas the model with the low-pass controller does not and is unstable. Because locomotor mechanics are similar in a wide array of animals, these data suggest that such high-pass sensory filters may be a general mechanism used for task-level locomotion control. Furthermore, these data highlight the critical role of mechanical analyses in addition to widely used kinematic analyses in the study of neural control systems.
The organization of the field L complex, a thalamorecipient auditory region in the telencephalon of birds, was examined in Nissl and Golgi preparations of male zebra finches (Taenopygia guttata). The field L complex comprises five cytoarchitectonic subdivisions: L1, L2a, L2b, L3, and L, although the border between L and L2b is not distinct. L2a is a plate extending dorsocaudally from the dorsal medullary lamina in the caudal neostriatum. L1 lies on the anterodorsal border and L3 lies on the posteroventral border of L2a. L, the area designated "field L" by Rose (J. Psychol. Neurol., 1914, 2:278-352), forms the medial and posterior borders of the field L complex. L2b is a thick band that forms the dorsal and dorsolateral boundary of the field L complex and is continuous with L medially. Nucleus interface (NIf) is a nucleus that lies between L2a and L1 near the lateral edge of the complex. The four types of Golgi stained neurons that occur in the zebra finch field L complex correspond to those described for the European starling (Sturnus vulgaris). Additionally, type 3 neurons are subdivided into "unoriented" neurons with spherical dendritic fields and "oriented" neurons with bipolar dendritic fields. NIf contains a distinct class of neurons that have large somata with both thick and thin spiny dendrites. The distribution of Golgi cell types between the subdivisions of the field L complex corresponds to the morphology of cells seen in Nissl material. Type 3 oriented cells are found almost exclusively within L2a. L3 has significantly greater numbers of the largest cells (type 1) and significantly smaller numbers of the smallest cells (type 4) than does L1. There are no significant differences in the distribution of Golgi stained cells between L2b and L.
SUMMARYPrevious work has shown that animals alter their locomotor behavior to increase sensing volumes. However, an animalʼs own movement also determines the spatial and temporal dynamics of sensory feedback. Because each sensory modality has unique spatiotemporal properties, movement has differential and potentially independent effects on each sensory system. Here we show that weakly electric fish dramatically adjust their locomotor behavior in relation to changes of modality-specific information in a task in which increasing sensory volume is irrelevant. We varied sensory information during a refuge-tracking task by changing illumination (vision) and conductivity (electroreception). The gain between refuge movement stimuli and fish tracking responses was functionally identical across all sensory conditions. However, there was a significant increase in the tracking error in the dark (no visual cues). This was a result of spontaneous whole-body oscillations (0.1 to 1Hz) produced by the fish. These movements were costly: in the dark, fish swam over three times further when tracking and produced more net positive mechanical work. The magnitudes of these oscillations increased as electrosensory salience was degraded via increases in conductivity. In addition, tail bending (1.5 to 2.35Hz), which has been reported to enhance electrosensory perception, occurred only during trials in the dark. These data show that both categories of movements -whole-body oscillations and tail bends -actively shape the spatiotemporal dynamics of electrosensory feedback. Supplementary material available online at
Plain-tailed wrens (Pheugopedius euophrys) cooperate to produce a duet song in which males and females rapidly alternate singing syllables. We examined how sensory information from each wren is used to coordinate singing between individuals for the production of this cooperative behavior. Previous findings in nonduetting songbird species suggest that premotor circuits should encode each bird's own contribution to the duet. In contrast, we find that both male and female wrens encode the combined cooperative output of the pair of birds. Further, behavior and neurophysiology show that both sexes coordinate the timing of their singing based on feedback from the partner and suggest that females may lead the duet.
Natural stimuli often have time-varying first-order (i.e., mean) and second-order (i.e., variance) attributes that each carry critical information for perception and can vary independently over orders of magnitude. Experiments have shown that sensory systems continuously adapt their responses based on changes in each of these attributes. This adaptation creates ambiguity in the neural code as multiple stimuli may elicit the same neural response. While parallel processing of first-and second-order attributes by separate neural pathways is sufficient to remove this ambiguity, the existence of such pathways and the neural circuits that mediate their emergence have not been uncovered to date. We recorded the responses of midbrain electrosensory neurons in the weakly electric fish Apteronotus leptorhynchus to stimuli with first-and second-order attributes that varied independently in time. We found three distinct groups of midbrain neurons: the first group responded to both first-and second-order attributes, the second group responded selectively to first-order attributes, and the last group responded selectively to second-order attributes. In contrast, all afferent hindbrain neurons responded to both first-and second-order attributes. Using computational analyses, we show how inputs from a heterogeneous population of ON-and OFF-type afferent neurons are combined to give rise to response selectivity to either first-or second-order stimulus attributes in midbrain neurons. Our study thus uncovers, for the first time, generic and widely applicable mechanisms by which parallel processing of first-and second-order stimulus attributes emerges in the brain.
SUMMARYThe weakly electric glass knifefish, Eigenmannia virescens, will swim forward and backward, using propulsion from an anal ribbon fin, in response to motion of a computer-controlled moving refuge. Fish were recorded performing a refuge-tracking behavior for sinusoidal (predictable) and sum-of-sines (pseudo-random) refuge trajectories. For all trials, we observed high coherence between refuge and fish trajectories, suggesting linearity of the tracking dynamics. But superposition failed: we observed categorical differences in tracking between the predictable single-sine stimuli and the unpredictable sum-of-sines stimuli. This nonlinearity suggests a stimulus-mediated adaptation. At all frequencies tested, fish demonstrated reduced tracking error when tracking single-sine trajectories and this was typically accompanied by a reduction in overall movement. Most notably, fish demonstrated reduced phase lag when tracking single-sine trajectories. These data support the hypothesis that fish generate an internal dynamical model of the stimulus motion, hence improving tracking of predictable trajectories (relative to unpredictable ones) despite similar or reduced motor cost. Similar predictive mechanisms based on the dynamics of stimulus movement have been proposed recently, but almost exclusively for nonlocomotor tasks by humans, such as oculomotor target tracking and posture control. These data suggest that such mechanisms might be common across taxa and behaviors.
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