Posterior parietal cortex represents sensory history and mediates its effects on behaviour.

Many models of cognition and of neural computations posit the use and estimation of prior stimulus statistics: it has long been known that working memory and perception are strongly impacted by previous sensory experience, even when that sensory history is not relevant to the current task at hand. Nevertheless, the neural mechanisms and regions of the brain that are necessary for computing and using such prior experience are unknown. Here we report that the posterior parietal cortex (PPC) is a critical locus for the representation and use of prior stimulus information. We trained rats in an auditory parametric working memory task, and found that they displayed substantial and readily quantifiable behavioural effects of sensory-stimulus history, similar to those observed in humans and monkeys. Earlier proposals that the PPC supports working memory predict that optogenetic silencing of this region would impair behaviour in our working memory task. Contrary to this prediction, we found that silencing the PPC significantly improved performance. Quantitative analyses of behaviour revealed that this improvement was due to the selective reduction of the effects of prior sensory stimuli. Electrophysiological recordings showed that PPC neurons carried far more information about the sensory stimuli of previous trials than about the stimuli of the current trial. Furthermore, for a given rat, the more information about previous trial sensory history in the neural firing rates of the PPC, the greater the behavioural effect of sensory history, suggesting a tight link between behaviour and PPC representations of stimulus history. Our results indicate that the PPC is a central component in the processing of sensory-stimulus history, and could enable further neurobiological investigation of long-standing questions regarding how perception and working memory are affected by prior sensory information.

Perceptual uncertainty.

The number of the distinct tactile percepts exceeds the number of receptor types in the skin, signifying that perception cannot be explained by a one-to-one mapping from a single receptor channel to a corresponding percept. The abundance of touch experiences results from multiplexing (the coexistence of multiple codes within a single channel, increasing the available information content of that channel) and from the mixture of receptor channels by divergence and convergence. When a neuronal representation emerges through the combination of receptor channels, perceptual uncertainty can occur-a perceptual judgment is affected by a stimulus feature that would be, ideally, excluded from the task. Though uncertainty seems at first glance to reflect nonoptimality in sensory processing, it is actually a consequence of efficient coding mechanisms that exploit prior knowledge about objects that are touched. Studies that analyze how perceptual judgments are "fooled" by variations in sensory input can reveal the neuronal mechanisms underlying the tactile experience.

A sensory integration account for time perception.

The connection between stimulus perception and time perception remains unknown. The present study combines human and rat psychophysics with sensory cortical neuronal firing to construct a computational model for the percept of elapsed time embedded within sense of touch. When subjects judged the duration of a vibration applied to the fingertip (human) or whiskers (rat), increasing stimulus intensity led to increasing perceived duration. Symmetrically, increasing vibration duration led to increasing perceived intensity. We modeled real spike trains recorded from vibrissal somatosensory cortex as input to dual leaky integrators-an intensity integrator with short time constant and a duration integrator with long time constant-generating neurometric functions that replicated the actual psychophysical functions of rats. Returning to human psychophysics, we then confirmed specific predictions of the dual leaky integrator model. This study offers a framework, based on sensory coding and subsequent accumulation of sensory drive, to account for how a feeling of the passage of time accompanies the tactile sensory experience.

Coherence between Rat Sensorimotor System and Hippocampus Is Enhanced during Tactile Discrimination.

Rhythms with time scales of multiple cycles per second permeate the mammalian brain, yet neuroscientists are not certain of their functional roles. One leading idea is that coherent oscillation between two brain regions facilitates the exchange of information between them. In rats, the hippocampus and the vibrissal sensorimotor system both are characterized by rhythmic oscillation in the theta range, 5-12 Hz. Previous work has been divided as to whether the two rhythms are independent or coherent. To resolve this question, we acquired three measures from rats--whisker motion, hippocampal local field potential (LFP), and barrel cortex unit firing--during a whisker-mediated texture discrimination task and during control conditions (not engaged in a whisker-mediated memory task). Compared to control conditions, the theta band of hippocampal LFP showed a marked increase in power as the rats approached and then palpated the texture. Phase synchronization between whisking and hippocampal LFP increased by almost 50% during approach and texture palpation. In addition, a greater proportion of barrel cortex neurons showed firing that was phase-locked to hippocampal theta while rats were engaged in the discrimination task. Consistent with a behavioral consequence of phase synchronization, the rats identified the texture more rapidly and with lower error likelihood on trials in which there was an increase in theta-whisking coherence at the moment of texture palpation. These results suggest that coherence between the whisking rhythm, barrel cortex firing, and hippocampal LFP is augmented selectively during epochs in which the rat collects sensory information and that such coherence enhances the efficiency of integration of stimulus information into memory and decision-making centers.

Sensory Prioritization in Rats: Behavioral Performance and Neuronal Correlates.

Operating with some finite quantity of processing resources, an animal would benefit from prioritizing the sensory modality expected to provide key information in a particular context. The present study investigated whether rats dedicate attentional resources to the sensory modality in which a near-threshold event is more likely to occur. We manipulated attention by controlling the likelihood with which a stimulus was presented from one of two modalities. In a whisker session, 80% of trials contained a brief vibration stimulus applied to whiskers and the remaining 20% of trials contained a brief change of luminance. These likelihoods were reversed in a visual session. When a stimulus was presented in the high-likelihood context, detection performance increased and was faster compared with the same stimulus presented in the low-likelihood context. Sensory prioritization was also reflected in neuronal activity in the vibrissal area of primary somatosensory cortex: single units responded differentially to the whisker vibration stimulus when presented with higher probability compared with lower probability. Neuronal activity in the vibrissal cortex displayed signatures of multiplicative gain control and enhanced response to vibration stimuli during the whisker session. In conclusion, rats allocate priority to the more likely stimulus modality and the primary sensory cortex may participate in the redistribution of resources. SIGNIFICANCE STATEMENT: Detection of low-amplitude events is critical to survival; for example, to warn prey of predators. To formulate a response, decision-making systems must extract minute neuronal signals from the sensory modality that provides key information. Here, we identify the behavioral and neuronal correlates of sensory prioritization in rats. Rats were trained to detect whisker vibrations or visual flickers. Stimuli were embedded in two contexts in which either visual or whisker modality was more likely to occur. When a stimulus was presented in the high-likelihood context, detection was faster and more reliable. Neuronal recording from the vibrissal cortex revealed enhanced representation of vibrations in the prioritized context. These results establish the rat as an alternative model organism to primates for studying attention.

Tactile perception and working memory in rats and humans.

Primates can store sensory stimulus parameters in working memory for subsequent manipulation, but until now, there has been no demonstration of this capacity in rodents. Here we report tactile working memory in rats. Each stimulus is a vibration, generated as a series of velocity values sampled from a normal distribution. To perform the task, the rat positions its whiskers to receive two such stimuli, "base" and "comparison," separated by a variable delay. It then judges which stimulus had greater velocity SD. In analogous experiments, humans compare two vibratory stimuli on the fingertip. We demonstrate that the ability of rats to hold base stimulus information (for up to 8 s) and their acuity in assessing stimulus differences overlap the performance demonstrated by humans. This experiment highlights the ability of rats to perceive the statistical structure of vibrations and reveals their previously unknown capacity to store sensory information in working memory.

Extracting information in spike time patterns with wavelets and information theory.

We present a new method to assess the information carried by temporal patterns in spike trains. The method first performs a wavelet decomposition of the spike trains, then uses Shannon information to select a subset of coefficients carrying information, and finally assesses timing information in terms of decoding performance: the ability to identify the presented stimuli from spike train patterns. We show that the method allows: 1) a robust assessment of the information carried by spike time patterns even when this is distributed across multiple time scales and time points; 2) an effective denoising of the raster plots that improves the estimate of stimulus tuning of spike trains; and 3) an assessment of the information carried by temporally coordinated spikes across neurons. Using simulated data, we demonstrate that the Wavelet-Information (WI) method performs better and is more robust to spike time-jitter, background noise, and sample size than well-established approaches, such as principal component analysis, direct estimates of information from digitized spike trains, or a metric-based method. Furthermore, when applied to real spike trains from monkey auditory cortex and from rat barrel cortex, the WI method allows extracting larger amounts of spike timing information. Importantly, the fact that the WI method incorporates multiple time scales makes it robust to the choice of partly arbitrary parameters such as temporal resolution, response window length, number of response features considered, and the number of available trials. These results highlight the potential of the proposed method for accurate and objective assessments of how spike timing encodes information.

Behavioral study of whisker-mediated vibration sensation in rats.

Rats use their vibrissal sensory system to collect information about the nearby environment. They can accurately and rapidly identify object location, shape, and surface texture. Which features of whisker motion does the sensory system extract to construct sensations? We addressed this question by training rats to make discriminations between sinusoidal vibrations simultaneously presented to the left and right whiskers. One set of rats learned to reliably identify which of two vibrations had higher frequency (f(1) vs. f(2)) when amplitudes were equal. Another set of rats learned to reliably identify which of two vibrations had higher amplitude (A(1) vs. A(2)) when frequencies were equal. Although these results indicate that both elemental features contribute to the rats' sensation, a further test found that the capacity to discriminate A and f was reduced to chance when the difference in one feature was counterbalanced by the difference in the other feature: Rats could not discriminate amplitude or frequency whenever A(1)f(1) = A(2)f(2). Thus, vibrations were sensed as the product Af rather than as separable elemental features, A and f. The product Af is proportional to a physical entity, the mean speed. Analysis of performance revealed that rats extracted more information about differences in Af than predicted by the sum of the information in elemental differences. These behavioral experiments support the predictions of earlier physiological studies by demonstrating that rats are "blind" to the elemental features present in a sinusoidal whisker vibration; instead, they perceive a composite feature, the speed of whisker motion.

Coordinated population activity underlying texture discrimination in rat barrel cortex.

Rodents can robustly distinguish fine differences in texture using their whiskers, a capacity that depends on neuronal activity in primary somatosensory "barrel" cortex. Here we explore how texture was collectively encoded by populations of three to seven neuronal clusters simultaneously recorded from barrel cortex while a rat performed a discrimination task. Each cluster corresponded to the single-unit or multiunit activity recorded at an individual electrode. To learn how the firing of different clusters combines to represent texture, we computed population activity vectors across moving time windows and extracted the signal available in the optimal linear combination of clusters. We quantified this signal using receiver operating characteristic analysis and compared it to that available in single clusters. Texture encoding was heterogeneous across neuronal clusters, and only a minority of clusters carried signals strong enough to support stimulus discrimination on their own. However, jointly recorded groups of clusters were always able to support texture discrimination at a statistically significant level, even in sessions where no individual cluster represented the stimulus. The discriminative capacity of neuronal activity was degraded when error trials were included in the data, compared to only correct trials, suggesting a link between the neuronal activity and the animal's performance. These analyses indicate that small groups of barrel cortex neurons can robustly represent texture identity through synergistic interactions, and suggest that neurons downstream to barrel cortex could extract texture identity on single trials through simple linear combination of barrel cortex responses.

Direct contribution of the sensory cortex to the judgment of stimulus duration.

Decision making frequently depends on monitoring the duration of sensory events. To determine whether, and how, the perception of elapsed time derives from the neuronal representation of the stimulus itself, we recorded and optogenetically modulated vibrissal somatosensory cortical activity as male rats judged vibration duration. Perceived duration was dilated by optogenetic excitation. A second set of rats judged vibration intensity; here, optogenetic excitation amplified the intensity percept, demonstrating sensory cortex to be the common gateway both to time and to stimulus feature processing. A model beginning with the membrane currents evoked by vibrissal and optogenetic drive and culminating in the representation of perceived time successfully replicated rats' choices. Time perception is thus as deeply intermeshed within the sensory processing pathway as is the sense of touch itself, suggesting that the experience of time may be further investigated with the toolbox of sensory coding.

'Where' and 'what' in the whisker sensorimotor system.

In the visual system of primates, different neuronal pathways are specialized for processing information about the spatial coordinates of objects and their identity - that is, 'where' and 'what'. By contrast, rats and other nocturnal animals build up a neuronal representation of 'where' and 'what' by seeking out and palpating objects with their whiskers. We present recent evidence about how the brain constructs a representation of the surrounding world through whisker-mediated sense of touch. While considerable knowledge exists about the representation of the physical properties of stimuli - like texture, shape and position - we know little about how the brain represents their meaning. Future research may elucidate this and show how the transformation of one representation to another is achieved.

Correlated physiological and perceptual effects of noise in a tactile stimulus.

We investigated connections between the physiology of rat barrel cortex neurons and the sensation of vibration in humans. One set of experiments measured neuronal responses in anesthetized rats to trains of whisker deflections, each train characterized either by constant amplitude across all deflections or by variable amplitude ("amplitude noise"). Firing rate and firing synchrony were, on average, boosted by the presence of noise. However, neurons were not uniform in their responses to noise. Barrel cortex neurons have been categorized as regular-spiking units (putative excitatory neurons) and fast-spiking units (putative inhibitory neurons). Among regular-spiking units, amplitude noise caused a higher firing rate and increased cross-neuron synchrony. Among fast-spiking units, noise had the opposite effect: It led to a lower firing rate and decreased cross-neuron synchrony. This finding suggests that amplitude noise affects the interaction between inhibitory and excitatory neurons. From these physiological effects, we expected that noise would lead to an increase in the perceived intensity of a vibration. We tested this notion using psychophysical measurements in humans. As predicted, subjects overestimated the intensity of noisy vibrations. Thus the physiological mechanisms present in barrel cortex also appear to be at work in the human tactile system, where they affect vibration perception.

Tactile cognition in rodents.

Since the discovery 50 years ago of the precisely ordered representation of the whiskers in somatosensory cortex, the rodent tactile sensory system has been a fertile ground for the study of sensory processing. With the growing sophistication of touch-based behavioral paradigms, together with advances in neurophysiological methodology, a new approach is emerging. By posing increasingly complex perceptual and memory problems, in many cases analogous to human psychophysical tasks, investigators now explore the operations underlying rodent problem solving. We define the neural basis of tactile cognition as the transformation from a stage in which neuronal activity encodes elemental features, local in space and in time, to a stage in which neuronal activity is an explicit representation of the behavioral operations underlying the current task. Selecting a set of whisker-based behavioral tasks, we show that rodents achieve high level performance through the workings of neuronal circuits that are accessible, decodable, and manipulatable. As a means towards exploring tactile cognition, this review presents leading psychophysical paradigms and, where known, their neural correlates.

Sound sensitivity of neurons in rat hippocampus during performance of a sound-guided task.

To investigate how hippocampal neurons encode sound stimuli, and the conjunction of sound stimuli with the animal's position in space, we recorded from neurons in the CA1 region of hippocampus in rats while they performed a sound discrimination task. Four different sounds were used, two associated with water reward on the right side of the animal and the other two with water reward on the left side. This allowed us to separate neuronal activity related to sound identity from activity related to response direction. To test the effect of spatial context on sound coding, we trained rats to carry out the task on two identical testing platforms at different locations in the same room. Twenty-one percent of the recorded neurons exhibited sensitivity to sound identity, as quantified by the difference in firing rate for the two sounds associated with the same response direction. Sensitivity to sound identity was often observed on only one of the two testing platforms, indicating an effect of spatial context on sensory responses. Forty-three percent of the neurons were sensitive to response direction, and the probability that any one neuron was sensitive to response direction was statistically independent from its sensitivity to sound identity. There was no significant coding for sound identity when the rats heard the same sounds outside the behavioral task. These results suggest that CA1 neurons encode sound stimuli, but only when those sounds are associated with actions.

When outgoing and incoming signals meet: new insights from the zona incerta.

In the sense of touch, it is the motion of the sensory receptors themselves that leads to an afferent signal-whether these receptors are in our fingertips sliding along a surface or a rat's whiskers palpating an object. Afferent signals can be correctly interpreted only if the sensory system receives information about the brain's own motor output. In this issue of Neuron, Urbain and Deschênes provide new insights into the physiological and anatomical interplay between tactile and motor signals in rats.

Unsupervised quantification of whisking and head movement in freely moving rodents.

The rodent whisker system has become the leading experimental paradigm for the study of active sensing. Thanks to more sophisticated behavioral paradigms, progressively better neurophysiological methods, and improved video hardware/software, there is now the prospect of defining the precise connection between the sensory apparatus and brain activity in awake, exploring animals. Achieving this ambitious goal requires quantitative, objective characterization of head and whisker kinematics. This study presents the methodology and potential uses of a new automated motion analysis routine. The program provides full quantification of head orientation and translation, as well as the angle, frequency, amplitude, and bilateral symmetry of whisking. The system operates without any need for manual tracing by the user. Quantitative comparison to whisker detection by expert humans indicates that the program's correct detection rate is at >95% even on animals with all whiskers intact. Particular attention has been paid to obtaining reliable performance under nonoptimal lighting or video conditions and at frame rates as low as 100. Variation of the zoom across time is compensated for without user intervention. The program adapts automatically to the size and shape of different species. The outcome of our testing indicates that the program can be a valuable tool in quantifying rodent sensorimotor behavior.

Conserved visual capacity of rats under red light.

Recent studies examine the behavioral capacities of rats and mice with and without visual input, and the neuronal mechanisms underlying such capacities. These animals are assumed to be functionally blind under red light, an assumption that might originate in the fact that they are dichromats who possess ultraviolet and green cones, but not red cones. But the inability to see red as a color does not necessarily rule out form vision based on red light absorption. We measured Long-Evans rats' capacity for visual form discrimination under red light of various wavelength bands. Upon viewing a black and white grating, they had to distinguish between two categories of orientation: horizontal and vertical. Psychometric curves plotting judged orientation versus angle demonstrate the conserved visual capacity of rats under red light. Investigations aiming to explore rodent physiological and behavioral functions in the absence of visual input should not assume red-light blindness.

Time coding in rat dorsolateral striatum.

To assess the role of dorsolateral striatum (DLS) in time coding, we recorded neuronal activity in rats tasked with comparing the durations of two sequential vibrations. Bayesian decoding of population activity revealed a representation of the unfolding of the trial across time. However, further analyses demonstrated a distinction between the encoding of trial time and perceived time. First, DLS did not show a privileged representation of the stimulus durations compared with other time spans. Second, higher intensity vibrations were perceived as longer; however, time decoded from DLS was unaffected by vibration intensity. Third, DLS did not encode stimulus duration differently on correct versus incorrect trials. Finally, in rats trained to compare the intensities of two sequential vibrations, stimulus duration was encoded even though it was a perceptually irrelevant feature. These findings lead us to posit that temporal information is inherent to DLS activity irrespective of the rat's ongoing percept.

Spine Surgery in Italy in the COVID-19 Era: Proposal for Assessing and Responding to the Regional State of Emergency.

In December 2019, coronavirus disease 2019 (COVID-19) was discovered in Wuhan, Hubei province, from where it spread rapidly worldwide. COVID-19 characteristics (increased infectivity, rapid spread, and general population susceptibility) pose a great challenge to hospitals. Infectious disease, pulmonology, and intensive care units have been strengthened and expanded. All other specialties have been compelled to suspend or reduce clinical and elective surgical activities. The profound effects on spine surgery call for systematic approaches to optimizing the diagnosis and treatment of spinal diseases. Based on the experience of one Italian region, we draw an archetype for assessing the current and predicted level of stress in the health care system, with the aim of enabling hospitals to make better decisions during the pandemic. Further, we provide a framework that may help guide strategies for adapting surgical spine care to the conditions of epidemic surge.