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Recently, a confluence between trends in neuroscience and machine learning has brought a renewed focus on unsupervised learning, where sensory processing systems learn to exploit the statistical structure of their inputs in the absence of explicit training targets or rewards. Sophisticated experimental approaches have enabled the investigation of the influence of sensory experience on neural self-organization and its synaptic bases. Meanwhile, novel algorithms for unsupervised and self-supervised learning have become increasingly popular both as inspiration for theories of the brain, particularly for the function of intermediate visual cortical areas, and as building blocks of real-world learning machines. Here we review some of these recent developments, placing them in historical context and highlighting some research lines that promise exciting breakthroughs in the near future.

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A key feature of advanced motion processing in the primate dorsal stream is the existence of pattern cells-specialized cortical neurons that integrate local motion signals into pattern-invariant representations of global direction. Pattern cells have also been reported in rodent visual cortex, but it is unknown whether the tuning of these neurons results from truly integrative, nonlinear mechanisms or trivially arises from linear receptive fields (RFs) with a peculiar geometry. Here, we show that pattern cells in rat primary (V1) and lateromedial (LM) visual cortex process motion direction in a way that cannot be explained by the linear spatiotemporal structure of their RFs. Instead, their tuning properties are consistent with and well explained by those of units in a state-of-the-art neural network model of the dorsal stream. This suggests that similar cortical processes underlay motion representation in primates and rodents. The latter could thus serve as powerful model systems to unravel the underlying circuit-level mechanisms.

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Behavioral states can influence performance of goal-directed sensorimotor tasks. Yet, it is unclear how altered neuronal sensory representations in these states relate to task performance and learning. We trained water-restricted mice in a two-whisker discrimination task to study cortical circuits underlying perceptual decision-making under different levels of thirst. We identified somatosensory cortices as well as the premotor cortex as part of the circuit necessary for task execution. Two-photon calcium imaging in these areas identified populations selective to sensory or motor events. Analysis of task performance during individual sessions revealed distinct behavioral states induced by decreasing levels of thirst-related motivation. Learning was better explained by improvements in motivational state control rather than sensorimotor association. Whisker sensory representations in the cortex were altered across behavioral states. In particular, whisker stimuli could be better decoded from neuronal activity during high task performance states, suggesting that state-dependent changes of sensory processing influence decision-making.

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Computing global motion direction of extended visual objects is a hallmark of primate high-level vision. Although neurons selective for global motion have also been found in mouse visual cortex, it remains unknown whether rodents can combine multiple motion signals into global, integrated percepts. To address this question, we trained two groups of rats to discriminate either gratings (G group) or plaids (i.e., superpositions of gratings with different orientations; P group) drifting horizontally along opposite directions. After the animals learned the task, we applied a visual priming paradigm, where presentation of the target stimulus was preceded by the brief presentation of either a grating or a plaid. The extent to which rat responses to the targets were biased by such prime stimuli provided a measure of the spontaneous, perceived similarity between primes and targets. We found that gratings and plaids, when used as primes, were equally effective at biasing the perception of plaid direction for the rats of the P group. Conversely, for the G group, only the gratings acted as effective prime stimuli, while the plaids failed to alter the perception of grating direction. To interpret these observations, we simulated a decision neuron reading out the representations of gratings and plaids, as conveyed by populations of either component or pattern cells (i.e., local or global motion detectors). We concluded that the findings for the P group are highly consistent with the existence of a population of pattern cells, playing a functional role similar to that demonstrated in primates. We also explored different scenarios that could explain the failure of the plaid stimuli to elicit a sizable priming magnitude for the G group. These simulations yielded testable predictions about the properties of motion representations in rodent visual cortex at the single-cell and circuitry level, thus paving the way to future neurophysiology experiments.

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In recent years, the advent of the so-called silicon probes has made it possible to homogeneously sample spikes and local field potentials (LFPs) from a regular grid of cortical recording sites. In principle, this allows inferring the laminar location of the sites based on the spatiotemporal pattern of LFPs recorded along the probe, as in the well-known current source-density (CSD) analysis. This approach, however, has several limitations, since it relies on visual identification of landmark features (i.e., current sinks and sources) by human operators - features that can be absent from the CSD pattern if the probe does not span the whole cortical thickness, thus making manual labelling harder. Furthermore, as any manual annotation procedure, the typical CSD-based workflow for laminar identification of recording sites is affected by subjective judgment undermining the consistency and reproducibility of results. To overcome these limitations, we developed an alternative approach, based on finding the optimal match between the LFPs recorded along a probe in a given experiment and a template LFP profile that was computed using 18 recording sessions, in which the depth of the recording sites had been recovered through histology. We show that this method can achieve an accuracy of 79 µm in recovering the cortical depth of recording sites and a 76% accuracy in inferring their laminar location. As such, our approach provides an alternative to CSD that, being fully automated, is less prone to the idiosyncrasies of subjective judgment and works reliably also for recordings spanning a limited cortical stretch.

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Unsupervised adaptation to the spatiotemporal statistics of visual experience is a key computational principle that has long been assumed to govern postnatal development of visual cortical tuning, including orientation selectivity of simple cells and position tolerance of complex cells in primary visual cortex (V1). Yet, causal empirical evidence supporting this hypothesis is scant. Here, we show that degrading the temporal continuity of visual experience during early postnatal life leads to a sizable reduction of the number of complex cells and to an impairment of their functional properties while fully sparing the development of simple cells. This causally implicates adaptation to the temporal structure of the visual input in the development of transformation tolerance but not of shape tuning, thus tightly constraining computational models of unsupervised cortical learning.

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In rodents, the progression of extrastriate areas located laterally to primary visual cortex (V1) has been assigned to a putative object-processing pathway (homologous to the primate ventral stream), based on anatomical considerations. Recently, we found functional support for such attribution (Tafazoli et al., 2017), by showing that this cortical progression is specialized for coding object identity despite view changes, the hallmark property of a ventral-like pathway. Here, we sought to clarify what computations are at the base of such specialization. To this aim, we performed multielectrode recordings from V1 and laterolateral area LL (at the apex of the putative ventral-like hierarchy) of male adult rats, during the presentation of drifting gratings and noise movies. We found that the extent to which neuronal responses were entrained to the phase of the gratings sharply dropped from V1 to LL, along with the quality of the receptive fields inferred through reverse correlation. Concomitantly, the tendency of neurons to respond to different oriented gratings increased, whereas the sharpness of orientation tuning declined. Critically, these trends are consistent with the nonlinear summation of visual inputs that is expected to take place along the ventral stream, according to the predictions of hierarchical models of ventral computations and a meta-analysis of the monkey literature. This suggests an intriguing homology between the mechanisms responsible for building up shape selectivity and transformation tolerance in the visual cortex of primates and rodents, reasserting the potential of the latter as models to investigate ventral stream functions at the circuitry level.SIGNIFICANCE STATEMENT Despite the growing popularity of rodents as models of visual functions, it remains unclear whether their visual cortex contains specialized modules for processing shape information. To addresses this question, we compared how neuronal tuning evolves from rat primary visual cortex (V1) to a downstream visual cortical region (area LL) that previous work has implicated in shape processing. In our experiments, LL neurons displayed a stronger tendency to respond to drifting gratings with different orientations while maintaining a sustained response across the whole duration of the drift cycle. These trends match the increased complexity of pattern selectivity and the augmented tolerance to stimulus translation found in monkey visual temporal cortex, thus revealing a homology between shape processing in rodents and primates.

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