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.

Development and Refinement of Functional Properties of Adult-Born Neurons.

October 17, 2017

Wallace JL, Wienisch M, Murthy VN

New neurons appear only in a few regions of the adult mammalian brain and become integrated into existing circuits. Little is known about the functional development of individual neurons in vivo. We examined the functional life history of adult-born granule cells (abGCs) in the olfactory bulb using multiphoton imaging in awake and anesthetized mice. We found that abGCs can become responsive to odorants soon after they arrive in the olfactory bulb. Tracking identified abGCs over weeks revealed that the robust and broadly tuned responses of most newly arrived abGCs gradually become more selective over a period of ∼3 weeks, but a small fraction achieves broader tuning with maturation. Enriching the olfactory environment of mice prolonged the period over which abGCs were strongly and broadly responsive to odorants. Our data offer direct support for rapid integration of adult-born neurons into existing circuits, followed by experience-dependent refinement of their functional connectivity.


Balanced excitation and inhibition are required for high-capacity, noise-robust neuronal selectivity.

October 17, 2017

Rubin R, Abbott LF, Sompolinsky H

Neurons and networks in the cerebral cortex must operate reliably despite multiple sources of noise. To evaluate the impact of both input and output noise, we determine the robustness of single-neuron stimulus selective responses, as well as the robustness of attractor states of networks of neurons performing memory tasks. We find that robustness to output noise requires synaptic connections to be in a balanced regime in which excitation and inhibition are strong and largely cancel each other. We evaluate the conditions required for this regime to exist and determine the properties of networks operating within it. A plausible synaptic plasticity rule for learning that balances weight configurations is presented. Our theory predicts an optimal ratio of the number of excitatory and inhibitory synapses for maximizing the encoding capacity of balanced networks for given statistics of afferent activations. Previous work has shown that balanced networks amplify spatiotemporal variability and account for observed asynchronous irregular states. Here we present a distinct type of balanced network that amplifies small changes in the impinging signals and emerges automatically from learning to perform neuronal and network functions robustly.

Active Mechanisms of Vibration Encoding and Frequency Filtering in Central Mechanosensory Neurons.

October 11, 2017

Azevedo AW, Wilson RI

To better understand biophysical mechanisms of mechanosensory processing, we investigated two cell types in the Drosophila brain (A2 and B1 cells) that are postsynaptic to antennal vibration receptors. A2 cells receive excitatory synaptic currents in response to both directions of movement: thus, twice per vibration cycle. The membrane acts as a low-pass filter, so that voltage and spiking mainly track the vibration envelope rather than individual cycles. By contrast, B1 cells are excited by only forward or backward movement, meaning they are sensitive to vibration phase. They receive oscillatory synaptic currents at the stimulus frequency, and they bandpass filter these inputs to favor specific frequencies. Different cells prefer different frequencies, due to differences in their voltage-gated conductances. Both Na+ and K + conductances suppress low-frequency synaptic inputs, so cells with larger voltage-gated conductances prefer higher frequencies. These results illustrate how membrane properties and voltage-gated conductances can extract distinct stimulus features into parallel channels.


Goal-Directed Visual Processing Differentially Impacts Human Ventral and Dorsal Visual Representations

September 6, 2017

Vaziri-Pashkam M, Xu Y

Recent studies have challenged the ventral/"what" and dorsal/"where" two-visual-processing-pathway view by showing the existence of "what" and "where" information in both pathways. Is the two-pathway distinction still valid? Here, we examined how goal-directed visual information processing may differentially impact visual representations in these two pathways. Using fMRI and multivariate pattern analysis, in three experiments on human participants (57% females), by manipulating whether color or shape was task-relevant and how they were conjoined, we examined shape-based object category decoding in occipitotemporal and parietal regions. We found that object category representations in all the regions examined were influenced by whether or not object shape was task-relevant. This task effect, however, tended to decrease as task-relevant and irrelevant features were more integrated, reflecting the well-known object-based feature encoding. Interestingly, task relevance played a relatively minor role in driving the representational structures of early visual and ventral object regions. They were driven predominantly by variations in object shapes. In contrast, the effect of task was much greater in dorsal than ventral regions, with object category and task relevance both contributing significantly to the representational structures of the dorsal regions. These results showed that, whereas visual representations in the ventral pathway are more invariant and reflect "what an object is," those in the dorsal pathway are more adaptive and reflect "what we do with it." Thus, despite the existence of "what" and "where" information in both visual processing pathways, the two pathways may still differ fundamentally in their roles in visual information representation.SIGNIFICANCE STATEMENT Visual information is thought to be processed in two distinctive pathways: the ventral pathway that processes "what" an object is and the dorsal pathway that processes "where" it is located. This view has been challenged by recent studies revealing the existence of "what" and "where" information in both pathways. Here, we found that goal-directed visual information processing differentially modulates shape-based object category representations in the two pathways. Whereas ventral representations are more invariant to the demand of the task, reflecting what an object is, dorsal representations are more adaptive, reflecting what we do with the object. Thus, despite the existence of "what" and "where" information in both pathways, visual representations may still differ fundamentally in the two pathways.