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Register a new userResponse and noise correlations to complex natural sounds in the auditory midbrain
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How natural communication sounds are spatially represented across the inferior colliculus, the main center of convergence for auditory information in the midbrain, is not known. The neural representation of the acoustic stimuli results from the interplay of locally differing input and the organization of spectral and temporal neural preferences that change gradually across the nucleus. This raises the question how similar the neural representation of the communication sounds is across these gradients of neural preferences, and whether it also changes gradually. Multi-unit cluster spike trains were recorded from guinea pigs presented with a spectrotemporally rich set of eleven species-specific communication sounds. Using cross-correlation, we analyzed the response similarity of spiking activity across a broad frequency range for similarly and differently frequency-tuned neurons. Furthermore, we separated the contribution of the stimulus to the correlations to investigate whether similarity is only attributable to the stimulus, or, whether interactions exist between the multi-unit clusters that lead to correlations and whether these follow the same representation as the response similarity. We found that similarity of responses is dependent on the neurons spatial distance for similarly and differently frequency-tuned neurons, and that similarity decreases gradually with spatial distance. Significant neural correlations exist, and contribute to the response similarity. Our findings suggest that for multi-unit clusters in the mammalian inferior colliculus, the gradual response similarity with spatial distance to natural complex sounds is shaped by neural interactions and the gradual organization of neural preferences.
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A central challenge in neuroscience is to understand neural computations and circuit mechanisms that underlie the encoding of ethologically relevant, natural stimuli. In multilayered neural circuits, nonlinear processes such as synaptic transmission and spiking dynamics present a significant obstacle to the creation of accurate computational models of responses to natural stimuli. Here we demonstrate that deep convolutional neural networks (CNNs) capture retinal responses to natural scenes nearly to within the variability of a cells response, and are markedly more accurate than linear-nonlinear (LN) models and Generalized Linear Models (GLMs). Moreover, we find two additional surprising properties of CNNs: they are less susceptible to overfitting than their LN counterparts when trained on small amounts of data, and generalize better when tested on stimuli drawn from a different distribution (e.g. between natural scenes and white noise). Examination of trained CNNs reveals several properties. First, a richer set of feature maps is necessary for predicting the responses to natural scenes compared to white noise. Second, temporally precise responses to slowly varying inputs originate from feedforward inhibition, similar to known retinal mechanisms. Third, the injection of latent noise sources in intermediate layers enables our model to capture the sub-Poisson spiking variability observed in retinal ganglion cells. Fourth, augmenting our CNNs with recurrent lateral connections enables them to capture contrast adaptation as an emergent property of accurately describing retinal responses to natural scenes. These methods can be readily generalized to other sensory modalities and stimulus ensembles. Overall, this work demonstrates that CNNs not only accurately capture sensory circuit responses to natural scenes, but also yield information about the circuits internal structure and function.
Natural images follow statistics inherited by the structure of our physical (visual) environment. In particular, a prominent facet of this structure is that images can be described by a relatively sparse number of features. To investigate the role of this sparseness in the efficiency of the neural code, we designed a new class of random textured stimuli with a controlled sparseness value inspired by measurements of natural images. Then, we tested the impact of this sparseness parameter on the firing pattern observed in a population of retinal ganglion cells recorded ex vivo in the retina of a rodent, the Octodon degus. These recordings showed in particular that the reliability of spike timings varies with respect to the sparseness with globally a similar trend than the distribution of sparseness statistics observed in natural images. These results suggest that the code represented in the spike pattern of ganglion cells may adapt to this aspect of the statistics of natural images.
The ongoing activity of neurons generates a spatially- and time-varying field of extracellular voltage ($V_e$). This $V_e$ field reflects population-level neural activity, but does it modulate neural dynamics and the function of neural circuits? We provide a cable theory framework to study how a bundle of model neurons generates $V_e$ and how this $V_e$ feeds back and influences membrane potential ($V_m$). We find that these ephaptic interactions are small but not negligible. The model neural population can generate $V_e$ with millivolt-scale amplitude and this $V_e$ perturbs the $V_m$ of nearby cables and effectively increases their electrotonic length. After using passive cable theory to systematically study ephaptic coupling, we explore a test case: the medial superior olive (MSO) in the auditory brainstem. The MSO is a possible locus of ephaptic interactions: sounds evoke large $V_e$ in vivo in this nucleus (millivolt-scale). The $V_e$ response is thought to be generated by MSO neurons that perform a known neuronal computation with submillisecond temporal precision (coincidence detection to encode sound source location). Using a biophysically-based model of MSO neurons, we find millivolt-scale ephaptic interactions consistent with the passive cable theory results. These subtle membrane potential perturbations induce changes in spike initiation threshold, spike time synchrony, and time difference sensitivity. These results suggest that ephaptic coupling may influence MSO function.
The relation between spontaneous and stimulated global brain activity is a fundamental problem in the understanding of brain functions. This question is investigated both theoretically and experimentally within the context of nonequilibrium fluctuation-dissipation relations. We consider the stochastic coarse-grained Wilson-Cowan model in the linear noise approximation and compare analytical results to experimental data from magnetoencephalography (MEG) of human brain. The short time behavior of the autocorrelation function for spontaneous activity is characterized by a double-exponential decay, with two characteristic times, differing by two orders of magnitude. Conversely, the response function exhibits a single exponential decay in agreement with experimental data for evoked activity under visual stimulation. Results suggest that the brain response to weak external stimuli can be predicted from the observation of spontaneous activity and pave the way to controlled experiments on the brain response under different external perturbations.
The role of the motor cortex in perceptual and cognitive functions is highly controversial. Here, we investigated the hypothesis that the motor cortex can be instrumental for translating foreign language vocabulary. Participants were trained on foreign language (L2) words and their native language translations over four consecutive days. L2 words were accompanied by complementary gestures (sensorimotor enrichment) or pictures (sensory enrichment). Following training, participants translated the auditorily-presented L2 words that they had learned and repetitive transcranial magnetic stimulation (rTMS) was applied to the bilateral posterior motor cortices. Compared to sham stimulation, effective perturbation by rTMS slowed down the translation of sensorimotor-enriched L2 words - but not sensory-enriched L2 words. This finding suggests that sensorimotor-enriched training induced changes in L2 representations within the motor cortex, which in turn facilitated the translation of L2 words. The motor cortex may play a causal role in precipitating sensorimotor-based learning benefits, and may directly aid in remembering the native language translations of foreign language words following sensorimotor-enriched training. These findings support multisensory theories of learning while challenging reactivation-based theories.
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