Understanding how neural populations encode sensory stimuli remains a central problem in neuroscience. Here we performed multi-unit recordings from sensory neural populations in the electrosensory ...system of the weakly electric fish Apteronotus leptorhynchus in response to stimuli located at different positions along the rostro-caudal axis. Our results reveal that the spatial dependence of correlated activity along receptive fields can help mitigate the deleterious effects that these correlations would otherwise have if they were spatially independent. Moreover, using mathematical modeling, we show that experimentally observed heterogeneities in the receptive fields of neurons help optimize information transmission as to object location. Taken together, our results have important implications for understanding how sensory neurons whose receptive fields display antagonistic center-surround organization encode location. Important similarities between the electrosensory system and other sensory systems suggest that our results will be applicable elsewhere.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Understanding how neural populations encode sensory information thereby leading to perception and behavior (i.e., the neural code) remains an important problem in neuroscience. When investigating the ...neural code, one must take into account the fact that neural activities are not independent but are actually correlated with one another. Such correlations are seen ubiquitously and have a strong impact on neural coding. Here we investigated how differences in the antagonistic center-surround receptive field (RF) organization across three parallel sensory maps influence correlations between the activities of electrosensory pyramidal neurons. Using a model based on known anatomical differences in receptive field center size and overlap, we initially predicted large differences in correlated activity across the maps. However, in vivo electrophysiological recordings showed that, contrary to modeling predictions, electrosensory pyramidal neurons across all three segments displayed nearly identical correlations. To explain this surprising result, we incorporated the effects of RF surround in our model. By systematically varying both the RF surround gain and size relative to that of the RF center, we found that multiple RF structures gave rise to similar levels of correlation. In particular, incorporating known physiological differences in RF structure between the three maps in our model gave rise to similar levels of correlation. Our results show that RF center overlap alone does not determine correlations which has important implications for understanding how RF structure influences correlated neural activity.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Understanding how neural populations encode natural stimuli with complex spatiotemporal structure to give rise to perception remains a central problem in neuroscience. Here we investigated population ...coding of natural communication stimuli by hindbrain neurons within the electrosensory system of weakly electric fish Apteronotus leptorhynchus. Overall, we found that simultaneously recorded neural activities were correlated: signal but not noise correlations were variable depending on the stimulus waveform as well as the distance between neurons. Combining the neural activities using an equal-weight sum gave rise to discrimination performance between different stimulus waveforms that was limited by redundancy introduced by noise correlations. However, using an evolutionary algorithm to assign different weights to individual neurons before combining their activities (i.e., a weighted sum) gave rise to increased discrimination performance by revealing synergistic interactions between neural activities. Our results thus demonstrate that correlations between the neural activities of hindbrain electrosensory neurons can enhance information about the structure of natural communication stimuli that allow for reliable discrimination between different waveforms by downstream brain areas.
There is accumulating evidence that the brain's neural coding strategies are constrained by natural stimulus statistics. Here we investigated the statistics of the time varying envelope (i.e. a ...second-order stimulus attribute that is related to variance) of rotational and translational self-motion signals experienced by human subjects during everyday activities. We found that envelopes can reach large values across all six motion dimensions (~450 deg/s for rotations and ~4 G for translations). Unlike results obtained in other sensory modalities, the spectral power of envelope signals decreased slowly for low (< 2 Hz) and more sharply for high (>2 Hz) temporal frequencies and thus was not well-fit by a power law. We next compared the spectral properties of envelope signals resulting from active and passive self-motion, as well as those resulting from signals obtained when the subject is absent (i.e. external stimuli). Our data suggest that different mechanisms underlie deviation from scale invariance in rotational and translational self-motion envelopes. Specifically, active self-motion and filtering by the human body cause deviation from scale invariance primarily for translational and rotational envelope signals, respectively. Finally, we used well-established models in order to predict the responses of peripheral vestibular afferents to natural envelope stimuli. We found that irregular afferents responded more strongly to envelopes than their regular counterparts. Our findings have important consequences for understanding the coding strategies used by the vestibular system to process natural second-order self-motion signals.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Natural sensory stimuli frequently consist of a fast time-varying waveform whose amplitude or contrast varies more slowly. While changes in contrast carry behaviorally relevant information necessary ...for sensory perception, their processing by the brain remains poorly understood to this day. Here, we investigated the mechanisms that enable neural responses to and perception of low-contrast stimuli in the electrosensory system of the weakly electric fish Apteronotus leptorhynchus. We found that fish reliably detected such stimuli via robust behavioral responses. Recordings from peripheral electrosensory neurons revealed stimulus-induced changes in firing activity (i.e., phase locking) but not in their overall firing rate. However, central electrosensory neurons receiving input from the periphery responded robustly via both phase locking and increases in firing rate. Pharmacological inactivation of feedback input onto central electrosensory neurons eliminated increases in firing rate but did not affect phase locking for central electrosensory neurons in response to low-contrast stimuli. As feedback inactivation eliminated behavioral responses to these stimuli as well, our results show that it is changes in central electrosensory neuron firing rate that are relevant for behavior, rather than phase locking. Finally, recordings from neurons projecting directly via feedback to central electrosensory neurons revealed that they provide the necessary input to cause increases in firing rate. Our results thus provide the first experimental evidence that feedback generates both neural and behavioral responses to low-contrast stimuli that are commonly found in the natural environment.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Correlations between the activities of neighboring neurons are observed ubiquitously across systems and species and are dynamically regulated by several factors such as the stimulus' spatiotemporal ...extent as well as by the brain's internal state. Using the electrosensory system of gymnotiform weakly electric fish, we recorded the activities of pyramidal cell pairs within the electrosensory lateral line lobe (ELL) under spatially localized and diffuse stimulation. We found that both signal and noise correlations were markedly reduced (>40%) under the latter stimulation. Through a network model incorporating key anatomical features of the ELL, we reveal how activation of diffuse parallel fiber feedback from granule cells by spatially diffuse stimulation can explain both the reduction in signal as well as the reduction in noise correlations seen experimentally through independent mechanisms. First, we show that burst-timing dependent plasticity, which leads to a negative image of the stimulus and thereby reduces single neuron responses, decreases signal but not noise correlations. Second, we show trial-to-trial variability in the responses of single granule cells to sensory input reduces noise but not signal correlations. Thus, our model predicts that the same feedback pathway can simultaneously reduce both signal and noise correlations through independent mechanisms. To test this prediction experimentally, we pharmacologically inactivated parallel fiber feedback onto ELL pyramidal cells. In agreement with modeling predictions, we found that inactivation increased both signal and noise correlations but that there was no significant relationship between magnitude of the increase in signal correlations and the magnitude of the increase in noise correlations. The mechanisms reported in this study are expected to be generally applicable to the cerebellum as well as other cerebellum-like structures. We further discuss the implications of such decorrelation on the neural coding strategies used by the electrosensory and by other systems to process natural stimuli.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
A prevailing view is that Weber's law constitutes a fundamental principle of perception. This widely accepted psychophysical law states that the minimal change in a given stimulus that can be ...perceived increases proportionally with amplitude and has been observed across systems and species in hundreds of studies. Importantly, however, Weber's law is actually an oversimplification. Notably, there exist violations of Weber's law that have been consistently observed across sensory modalities. Specifically, perceptual performance is better than that predicted from Weber's law for the higher stimulus amplitudes commonly found in natural sensory stimuli. To date, the neural mechanisms mediating such violations of Weber's law in the form of improved perceptual performance remain unknown. Here, we recorded from vestibular thalamocortical neurons in rhesus monkeys during self-motion stimulation. Strikingly, we found that neural discrimination thresholds initially increased but saturated for higher stimulus amplitudes, thereby causing the improved neural discrimination performance required to explain perception. Theory predicts that stimulus-dependent neural variability and/or response nonlinearities will determine discrimination threshold values. Using computational methods, we thus investigated the mechanisms mediating this improved performance. We found that the structure of neural variability, which initially increased but saturated for higher amplitudes, caused improved discrimination performance rather than response nonlinearities. Taken together, our results reveal the neural basis for violations of Weber's law and further provide insight as to how variability contributes to the adaptive encoding of natural stimuli with continually varying statistics.
How the activities of large neural populations are integrated in the brain to ensure accurate perception and behavior remains a central problem in systems neuroscience. Here, we investigated ...population coding of naturalistic self-motion by neurons within early vestibular pathways in rhesus macaques (Macacca mulatta). While vestibular neurons displayed similar dynamic tuning to self-motion, inspection of their spike trains revealed significant heterogeneity. Further analysis revealed that, during natural but not artificial stimulation, heterogeneity resulted primarily from variability across neurons as opposed to trial-to-trial variability. Interestingly, vestibular neurons displayed different correlation structures during naturalistic and artificial self-motion. Specifically, while correlations due to the stimulus (i.e., signal correlations) did not differ, correlations between the trial-to-trial variabilities of neural responses (i.e., noise correlations) were instead significantly positive during naturalistic but not artificial stimulation. Using computational modeling, we show that positive noise correlations during naturalistic stimulation benefits information transmission by heterogeneous vestibular neural populations. Taken together, our results provide evidence that neurons within early vestibular pathways are adapted to the statistics of natural self-motion stimuli at the population level. We suggest that similar adaptations will be found in other systems and species.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
It is widely believed that sensory systems are optimized for processing stimuli occurring in the natural environment. However, it remains unknown whether this principle applies to the vestibular ...system, which contributes to essential brain functions ranging from the most automatic reflexes to spatial perception and motor coordination. Here we quantified, for the first time, the statistics of natural vestibular inputs experienced by freely moving human subjects during typical everyday activities. Although previous studies have found that the power spectra of natural signals across sensory modalities decay as a power law (i.e., as 1/f(α)), we found that this did not apply to natural vestibular stimuli. Instead, power decreased slowly at lower and more rapidly at higher frequencies for all motion dimensions. We further establish that this unique stimulus structure is the result of active motion as well as passive biomechanical filtering occurring before any neural processing. Notably, the transition frequency (i.e., frequency at which power starts to decrease rapidly) was lower when subjects passively experienced sensory stimulation than when they actively controlled stimulation through their own movement. In contrast to signals measured at the head, the spectral content of externally generated (i.e., passive) environmental motion did follow a power law. Specifically, transformations caused by both motor control and biomechanics shape the statistics of natural vestibular stimuli before neural processing. We suggest that the unique structure of natural vestibular stimuli will have important consequences on the neural coding strategies used by this essential sensory system to represent self-motion in everyday life.
Sensory systems must continuously adapt to optimally encode stimuli encountered within the natural environment. The prevailing view is that such optimal coding comes at the cost of increased ...ambiguity, yet to date, prior studies have focused on artificial stimuli. Accordingly, here we investigated whether such a trade-off between optimality and ambiguity exists in the encoding of natural stimuli in the vestibular system. We recorded vestibular nuclei and their target vestibular thalamocortical neurons during naturalistic and artificial self-motion stimulation. Surprisingly, we found no trade-off between optimality and ambiguity. Using computational methods, we demonstrate that thalamocortical neural adaptation in the form of contrast gain control actually reduces coding ambiguity without compromising the optimality of coding under naturalistic but not artificial stimulation. Thus, taken together, our results challenge the common wisdom that adaptation leads to ambiguity and instead suggest an essential role in underlying unambiguous optimized encoding of natural stimuli.
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