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Visual discrimination and amodal completion in zebrafish
While zebrafish represent an important model for the study of the visual system, visual perception in this species is still less investigated than in other teleost fish. In this work, we validated for zebrafish two versions of a visual discrimination learning task, which is based on the motivation to reach food and companions. Using this task, we investigated zebrafish ability to discriminate between two different shape pairs (i.e., disk vs. cross and full vs. amputated disk). Once zebrafish were successfully trained to discriminate a full from an amputated disk, we also tested their ability to visually complete partially occluded objects (amodal completion). After training, animals were presented with two amputated disks. In these test stimuli, another shape was either exactly juxtaposed or only placed close to the missing sectors of the disk. Only the former stimulus should elicit amodal completion. In human observers, this stimulus causes the impression that the other shape is occluding the missing sector of the disk, which is thus perceived as a complete, although partially hidden, disk. In line with our predictions, fish reinforced on the full disk chose the stimulus eliciting amodal completion, while fish reinforced on the amputated disk chose the other stimulus. This represents the first demonstration of amodal completion perception in zebrafish. Moreover, our results also indicated that a specific shape pair (disk vs. cross) might be particularly difficult to discriminate for this species, confirming previous reports obtained with different procedures.
Journal Article
Distinct learning-induced changes in stimulus selectivity and interactions of GABAergic interneuron classes in visual cortex
How learning enhances neural representations for behaviorally relevant stimuli via activity changes of cortical cell types remains unclear. We simultaneously imaged responses of pyramidal cells (PYR) along with parvalbumin (PV), somatostatin (SOM), and vasoactive intestinal peptide (VIP) inhibitory interneurons in primary visual cortex while mice learned to discriminate visual patterns. Learning increased selectivity for task-relevant stimuli of PYR, PV and SOM subsets but not VIP cells. Strikingly, PV neurons became as selective as PYR cells, and their functional interactions reorganized, leading to the emergence of stimulus-selective PYR–PV ensembles. Conversely, SOM activity became strongly decorrelated from the network, and PYR–SOM coupling before learning predicted selectivity increases in individual PYR cells. Thus, learning differentially shapes the activity and interactions of multiple cell classes: while SOM inhibition may gate selectivity changes, PV interneurons become recruited into stimulus-specific ensembles and provide more selective inhibition as the network becomes better at discriminating behaviorally relevant stimuli.
Journal Article
Mouse visual cortex areas represent perceptual and semantic features of learned visual categories
Associative memories are stored in distributed networks extending across multiple brain regions. However, it is unclear to what extent sensory cortical areas are part of these networks. Using a paradigm for visual category learning in mice, we investigated whether perceptual and semantic features of learned category associations are already represented at the first stages of visual information processing in the neocortex. Mice learned categorizing visual stimuli, discriminating between categories and generalizing within categories. Inactivation experiments showed that categorization performance was contingent on neuronal activity in the visual cortex. Long-term calcium imaging in nine areas of the visual cortex identified changes in feature tuning and category tuning that occurred during this learning process, most prominently in the postrhinal area (POR). These results provide evidence for the view that associative memories form a brain-wide distributed network, with learning in early stages shaping perceptual representations and supporting semantic content downstream.
Goltstein et al. investigate the role of mouse visual cortical areas in information-integration category learning. They report widespread changes in neuronal response properties, most prominently in a higher visual area, the postrhinal cortex.
Journal Article
Microglia and complement mediate early corticostriatal synapse loss and cognitive dysfunction in Huntington’s disease
Huntington’s disease (HD) is a devastating monogenic neurodegenerative disease characterized by early, selective pathology in the basal ganglia despite the ubiquitous expression of mutant huntingtin. The molecular mechanisms underlying this region-specific neuronal degeneration and how these relate to the development of early cognitive phenotypes are poorly understood. Here we show that there is selective loss of synaptic connections between the cortex and striatum in postmortem tissue from patients with HD that is associated with the increased activation and localization of complement proteins, innate immune molecules, to these synaptic elements. We also found that levels of these secreted innate immune molecules are elevated in the cerebrospinal fluid of premanifest HD patients and correlate with established measures of disease burden.
In preclinical genetic models of HD, we show that complement proteins mediate the selective elimination of corticostriatal synapses at an early stage in disease pathogenesis, marking them for removal by microglia, the brain’s resident macrophage population. This process requires mutant huntingtin to be expressed in both cortical and striatal neurons. Inhibition of this complement-dependent elimination mechanism through administration of a therapeutically relevant C1q function-blocking antibody or genetic ablation of a complement receptor on microglia prevented synapse loss, increased excitatory input to the striatum and rescued the early development of visual discrimination learning and cognitive flexibility deficits in these models. Together, our findings implicate microglia and the complement cascade in the selective, early degeneration of corticostriatal synapses and the development of cognitive deficits in presymptomatic HD; they also provide new preclinical data to support complement as a therapeutic target for early intervention.
Microglia mediate the early and selective degeneration of corticostriatal synapses and the development of cognitive deficits in presymptomatic Huntington’s disease via the complement cascade.
Journal Article
Visual discrimination training increases the speed stimulus processing and leads to an earlier onset of stimulus encoding
Wide experience with complex visual stimuli results in better performance and faster responses in object discrimination, categorization, and identification through perceptual learning and expertise. Visual experts exhibit an earlier onset of the availability of stimulus information for encoding and a reduction of the encoding duration required for discrimination and individuation. However, it is still unresolved whether perceptual learning and expertise shapes the speed of perceptual processing in the first milliseconds after stimulus onset. Twenty seven participants developed perceptual learning and expertise through discrimination of pairs of Kanji stimuli across six sessions. Discrimination sensitivity was evaluated at four training levels with encoding durations between 17 and 1000 ms. Behavioral results show a gradual increase in sensitivity and a reduction in encoding duration required for a given performance with discrimination training. A shifted exponential function fitted to the sensitivity data revealed that training leads to a faster rate of performance change with encoding durations, suggesting increases in the speed of information extraction, as well as an earlier availability of stimulus information for encoding, suggesting an earlier onset of information extraction. Interestingly, the increase in the rate of performance paralleled that of sensitivity with training, suggesting an association with perceptual learning and expertise. Besides, the earlier availability of stimulus information is achieved after two training sessions, likely reflecting the acquisition of stimuli familiarity. The faster speed of information extraction and the earlier stimulus information extraction for encoding, likely contribute to faster responses and higher performance, typical of perceptual experts in object discrimination and individuation. These findings provide additional evidence for the outcome of discrimination training on stimulus processing in the first milliseconds after stimulus onset.
Journal Article
Multisensory stimuli facilitate low-level perceptual learning on a difficult global motion task in virtual reality
The present study investigates the feasibility of inducing visual perceptual learning on a peripheral, global direction discrimination and integration task in virtual reality, and tests whether audio-visual multisensory training induces faster or greater visual learning than unisensory visual training. Seventeen participants completed a 10-day training experiment wherein they repeatedly performed a 4-alternative, combined visual global-motion and direction discrimination task at 10° azimuth/elevation in a virtual environment. A visual-only group of 8 participants was trained using a unimodal visual stimulus. An audio-visual group of 9 participants underwent training whereby the visual stimulus was always paired with a pulsed, white-noise auditory cue that simulated auditory motion in a direction consistent with the horizontal component of the visual motion stimulus. Our results reveal that, for both groups, learning occurred and transferred to untrained locations. For the AV group, there was an additional performance benefit to training from the AV cue to horizontal motion. This benefit extended into the unisensory post-test, where the auditory cue was removed. However, this benefit did not generalize spatially to previously untrained areas. This spatial specificity suggests that AV learning may have occurred at a lower level in the visual pathways, compared to visual-only learning.
Journal Article
Time courses of brain plasticity underpinning visual motion perceptual learning
•VPL increased neural selectivity for the trained motion direction, as evidenced by improved decoding accuracy.•VPL reduced the motion direction decoding latency.•Training enhanced the cortical response in EVC and strengthened the feedforward connection from EVC to V3A.•The changes in neural selectivity and EVC response amplitude co-occurred between 160 and 230 ms post-stimulus.
Visual perceptual learning (VPL) refers to a long-term improvement of visual task performance through training or experience, reflecting brain plasticity even in adults. In human subjects, VPL has been mostly studied using functional magnetic resonance imaging (fMRI). However, due to the low temporal resolution of fMRI, how VPL affects the time course of visual information processing is largely unknown. To address this issue, we trained human subjects to perform a visual motion direction discrimination task. Their behavioral performance and magnetoencephalography (MEG) signals responding to the motion stimuli were measured before, immediately after, and two weeks after training. Training induced a long-lasting behavioral improvement for the trained direction. Based on the MEG signals from occipital sensors, we found that, for the trained motion direction, VPL increased the motion direction decoding accuracy, reduced the motion direction decoding latency, enhanced the direction-selective channel response, and narrowed the tuning profile. Following the MEG source reconstruction, we showed that VPL enhanced the cortical response in early visual cortex (EVC) and strengthened the feedforward connection from EVC to V3A. These VPL-induced neural changes co-occurred in 160–230 ms after stimulus onset. Complementary to previous fMRI findings on VPL, this study provides a comprehensive description on the neural mechanisms of visual motion perceptual learning from a temporal perspective and reveals how VPL shapes the time course of visual motion processing in the adult human brain.
Journal Article
An essential role for the latero-medial secondary visual cortex in the acquisition and retention of visual perceptual learning in mice
Perceptual learning refers to any change in discrimination abilities as a result of practice, a fundamental process that improves the organism’s response to the external environment. Visual perceptual learning (vPL) is supposed to rely on functional rearrangements in brain circuity occurring at early stages of sensory processing, with a pivotal role for the primary visual cortex (V1). However, top-down inputs from higher-order visual areas (HVAs) have been suggested to play a key part in vPL, conveying information on attention, expectation and the precise nature of the perceptual task. A direct assessment of the possibility to modulate vPL by manipulating top-down activity in awake subjects is still missing. Here, we used a combination of chemogenetics, behavioral analysis and multichannel electrophysiological assessments to show a critical role in vPL acquisition and retention for neuronal activity in the latero-medial secondary visual cortex (LM), the prime source for top-down feedback projections reentering V1.
While information conveyed to the primary visual cortex (V1) by top-down signals is thought to be required for visual perceptual learning, it remains unknown whether it is possible to modulate visual perceptual learning by manipulating top-down neuronal activity. Here the authors employ a mouse model of visual perceptual learning in a forced-choice visual discrimination task to demonstrate an essential role of the latero-medial secondary visual cortex, the prime source for top-down feedback projections reentering V1.
Journal Article
What the visual system can learn from the non-dominant hand: The effect of graphomotor engagement on visual discrimination
Previous studies have demonstrated that engaging in graphomotor activity for creating graphemes can enhance their subsequent visual discrimination. This suggests a positive influence of the motor system on visual learning. However, existing studies have emphasized the dominant hand, which is superiorly dexterous in fine-motor movements. This near-exclusive focus prompts the inquiry of whether the observed perceptual facilitation is a general characteristic of the motor system, or specific to pathways controlling the skilled over-trained dominant hand. Furthermore, the mechanistic underpinning of visual facilitation from graphomotor training (i.e., the individual contribution of motor activity, temporal evolution of the visual trace, variability of visual output) remain unclear. To address these questions, we assessed visual discrimination capabilities of healthy right-handed participants (N = 60) before and after graphomotor or visual training. Contrary to our initial expectation, graphomotor engagement with the non-dominant hand did not yield additional benefits to visual learning beyond those attainable through visual training alone. Moreover, graphomotor training with the non-dominant hand resulted in visual discrimination improvements comparable to those of dominant hand training, despite the inherent differences between hands in motor performance and in the amount of improvement in shape tracing throughout training. We conclude that the motor components of graphomotor activity may not be critical for visual learning of shapes through tracing activity. Instead, our results are in agreement with the symbolic theoretical account, suggesting that basic shape features required for discrimination can be acquired through visual inspection alone, providing a perspective on the improvements observed in prior studies.
Journal Article