Alternation of Neuronal Feature Selectivity Induced by Paired Optogenetic-Mechanical Stimulation in the Barrel Cortex

Paired stimulation has been applied to modulate neuronal functions in the primary somatosensory cortex but its utility in the alternation of tuning function, such as direction tuning for whisker stimuli, remains unclear. In the present study, we attempted to manipulate feature preferences in barrel cortical neurons using repetitive paired whisker deflection combined with optogenetic stimulation and to obtain optimal parameters that can induce neuroplasticity. We found no significant response changes across stimulus parameters, such as onset asynchronies and paired directions. Only when paired stimulation was applied in the nonpreferred direction of the principal whisker of a neuron, were the neuron’s responses enhanced in that direction. Importantly, this effect was only observed when the optogenetic stimulus preceded the mechanical stimulus. Our findings indicate that repetitive paired optogenetic-mechanical stimulation can induce in vivo neuroplasticity of feature selectivity in limited situations.

Spatially structured inhibition defined by polarized parvalbumin interneuron axons promotes head direction tuning

In cortical microcircuits, it is generally assumed that fast-spiking parvalbumin interneurons mediate dense and nonselective inhibition. Some reports indicate sparse and structured inhibitory connectivity, but the computational relevance and the underlying spatial organization remain unresolved. In the rat superficial presubiculum, we find that inhibition by fast-spiking interneurons is organized in the form of a dominant super-reciprocal microcircuit motif where multiple pyramidal cells recurrently inhibit each other via a single interneuron. Multineuron recordings and subsequent 3D reconstructions and analysis further show that this nonrandom connectivity arises from an asymmetric, polarized morphology of fast-spiking interneuron axons, which individually cover different directions in the same volume. Network simulations assuming topographically organized input demonstrate that such polarized inhibition can improve head direction tuning of pyramidal cells in comparison to a “blanket of inhibition.” We propose that structured inhibition based on asymmetrical axons is an overarching spatial connectivity principle for tailored computation across brain regions.

The Serpentine Illusion: A Visual Motion Illusion Induced by Phase-Shifted Line Gratings

In a pattern of horizontal lines containing ± 45° zigzagging phase-shifted strips, vivid illusory motion is perceived when the pattern is translated up or down at a moderate speed. Two forms of illusory motion are seen: [i] a motion “racing” along the diagonal interface between the strips and [ii] lateral (sideways) motion of the strip sections. We found the relative salience of these two illusory motions to be strongly influenced by the vertical spacing and length of the line gratings, and the period length of the zigzag strips. Both illusory motions are abolished when the abutting strips are interleaved, separated by a gap or when a real line is superimposed at the interface. Illusory motion is also severely weakened when equiluminant colored grating lines are used. Illusory motion perception is fully restored at < 20% luminance contrast. Using adaptation, we find that line-ends alone are insufficient for illusory motion perception, and that both physical carrier motion and line orientation are required. We finally test a classical spatiotemporal energy model of V1 cells that exhibit direction tuning changes that are consistent with the direction of illusory motion. Taking this data together, we constructed a new visual illusion and surmise its origin to interactions of spatial and temporal energy of the lines and line-ends preferentially driving the magnocellular pathway.

Impaired speed encoding and grid cell periodicity in a mouse model of tauopathy

Dementia is associated with severe spatial memory deficits which arise from dysfunction in hippocampal and parahippocampal circuits. For spatially sensitive neurons, such as grid cells, to faithfully represent the environment these circuits require precise encoding of direction and velocity information. Here, we have probed the firing rate coding properties of neurons in medial entorhinal cortex (MEC) in a mouse model of tauopathy. We find that grid cell firing patterns are largely absent in rTg4510 mice, while head-direction tuning remains largely intact. Conversely, neural representation of running speed information was significantly disturbed, with smaller proportions of MEC cells having firing rates correlated with locomotion in rTg4510 mice. Additionally, the power of local field potential oscillations in the theta and gamma frequency bands, which in wild-type mice are tightly linked to running speed, was invariant in rTg4510 mice during locomotion. These deficits in locomotor speed encoding likely severely impact path integration systems in dementia.

A cortico-collicular circuit for accurate orientation to shelter during escape

When faced with predatorial threats, escaping towards shelter is an adaptive action that offers long-term protection against the attacker. From crustaceans to mammals, animals rely on knowledge of safe locations in the environment to rapidly execute shelter-directed escape actions1–3. While previous work has identified neural mechanisms of instinctive escape4–9, it is not known how the escape circuit incorporates spatial information to execute rapid and accurate flights to safety. Here we show that mouse retrosplenial cortex (RSP) and superior colliculus (SC) form a monosynaptic circuit that continuously encodes the shelter direction. Inactivation of SC-projecting RSP neurons decreases SC shelter-direction tuning while preserving SC motor function. Moreover, specific inactivation of RSP input onto SC neurons disrupts orientation and subsequent escapes to shelter, but not orientation accuracy to a sensory cue. We conclude that the RSC-SC circuit supports an egocentric representation of shelter direction and is necessary for optimal shelter-directed escapes. This cortical-subcortical interface may be a general blueprint for increasing the sophistication and flexibility of instinctive behaviours.

Dynamic control of cortical head-direction signal by angular velocity

The sense of direction requires accurate tracking of head direction at different turning-velocities, yet it remains unclear how this is achieved in the mammalian brain. Here we recorded head-direction cells in bat dorsal presubiculum and found that, surprisingly, the head-direction signal in this cortical region was dynamically controlled by angular velocity. In most neurons, a sharp head-direction tuning emerged at some angular velocity, but was absent at other velocities – resulting in a 4-fold increase in head-direction cell abundance. The head-direction tuning changed as a function of angular velocity primarily via a redistribution of spikes between the neuron’s preferred and null directions – while keeping the average firing-rate constant. These results could not be explained by existing ‘ring-attractor’ models of the head-direction system. We propose a novel recurrent network model that accounts for the observed dynamics of head-direction cells. This model predicts that the new classes of cells we found can improve the sensitivity of the head-direction system to directional sensory cues, and support angular-velocity integration.

Impaired speed encoding is associated with reduced grid cell periodicity in a mouse model of tauopathy

Dementia is associated with severe spatial memory deficits which arise from dysfunction in hippocampal and parahippocampal circuits. For spatially-sensitive neurons, such as grid cells, to faithfully represent the environment these circuits require precise encoding of direction and velocity information. Here we have probed the firing rate coding properties of neurons in medial entorhinal cortex (MEC) in a mouse model of tauopathy. We find that grid cell firing patterns are largely absent in rTg4510 mice, while head direction tuning remains largely intact. Conversely, neural representation of running speed information was significantly disturbed, with smaller proportions of MEC cells having firing rates correlated with locomotion in rTg4510 mice. Additionally, the power of local field potential oscillations in the theta and gamma frequency bands, which in wildtype mice are tightly linked to running speed, was invariant in rTg4510 mice. These deficits in locomotor speed encoding likely severely impact path integration systems in dementia.

Motion direction representation in multivariate electroencephalography activity for smooth pursuit eye movements

Visually-guided smooth pursuit eye movements are composed of initial open-loop and later steady-state periods. Feedforward sensory information dominates the motor behavior during the open-loop pursuit, and a more complex feedback loop regulates the steady-state pursuit. To understand the neural representations of motion direction during open-loop and steady-state smooth pursuits, we recorded electroencephalography (EEG) responses from human observers while they tracked random dot kinematograms as pursuit targets. We estimated population direction tuning curves from multivariate EEG activity using an inverted encoding model. We found significant direction tuning curves as early as 20 ms from motion onset. Direction tuning responses were generalized to later times during the open-loop smooth pursuit, but they became more dynamic during the later steady-state pursuit. The encoding quality of retinal motion direction information estimated from the early direction tuning curves was predictive of trial-by-trial variation in initial pursuit directions. These results suggest that the movement directions of open-loop smooth pursuit are guided by the representation of the retinal motion present in the multivariate EEG activity.