Brain function involves the activity of neuronal populations. Much recent effort has been devoted to measuring the activity of neuronal populations in different parts of the brain under various experimental conditions. Population activity patterns contain rich structure, yet many studies have focused on measuring pairwise relationships between members of a larger population---termed noise correlations. Here we review recent progress in understanding how these correlations affect population information, how information should be quantified, and what mechanisms may give rise to correlations. As population coding theory has improved, it has made clear that some forms of correlation are more important for information than others. We argue that this is a critical lesson for those interested in neuronal population responses more generally: Descriptions of population responses should be motivated by and linked to well-specified function. Within this context, we offer suggestions of where current theoretical frameworks fall short.
Identical sensory inputs can be perceived as strikingly different when embedded in distinct contexts. Neural responses to simple stimuli are also modulated by context, but the contribution of this modulation to the processing of natural sensory input is unclear. We measured surround suppression, a quintessential contextual influence, in macaque primary visual cortex with natural images. We found suppression strength varied substantially for different images. This variability was not well explained by existing descriptions of surround suppression, but it was predicted by Bayesian inference about statistical dependencies in images. In this framework, surround suppression was flexible: it was recruited when the image was inferred to contain redundancies, and substantially reduced in strength otherwise. Our results thus reveal a surprising gating of a basic, widespread cortical computation, by inference about the statistics of natural input.
The ability to discriminate between similar sensory stimuli relies on the amount of information encoded in sensory neuronal populations. Such information can be substantially reduced by correlated trial-to-trial variability. Noise correlations have been measured across a wide range of areas in the brain, but their origin is still far from clear. Here we show analytically and with simulations that optimal computation on inputs with limited information creates patterns of noise correlations that account for a broad range of experimental observations while at same time causing information to saturate in large neural populations. With the example of a network of V1 neurons extracting orientation from a noisy image, we illustrate to our knowledge the first generative model of noise correlations that is consistent both with neurophysiology and with behavioral thresholds, without invoking suboptimal encoding or decoding or internal sources of variability such as stochastic network dynamics or cortical state fluctuations. We further show that when information is limited at the input, both suboptimal connectivity and internal fluctuations could similarly reduce the asymptotic information, but they have qualitatively different effects on correlations leading to specific experimental predictions. Our study indicates that noise at the sensory periphery could have a major effect on cortical representations in widely studied discrimination tasks. It also provides an analytical framework to understand the functional relevance of different sources of experimentally measured correlations.noise correlations | information theory | neural computation | efficient coding | neuronal variability T he response of cortical neurons to an identical stimulus varies from trial to trial. Moreover, this variability tends to be correlated among pairs of nearby neurons. These correlations, known as noise correlations, have been the subject of numerous experimental as well as theoretical studies because they can have a profound impact on behavioral performance (1-7). Indeed, behavioral performance in discrimination tasks is inversely proportional to the Fisher information available in the neural responses, which itself is strongly dependent on the pattern of correlations. In particular, correlations can strongly limit information in the sense that some patterns of correlations can lead information to saturate to a finite value in large populations, in sharp contrast to the case of independent neurons for which information grows proportionally to the number of neurons. However, the saturation is observed for only one type of correlations known as differential correlations. If the correlation pattern slightly deviates from differential correlations, information typically scales with the number of neurons, just like it does for independent neurons (7). These previous results clarify how correlations impact information and consequently behavioral performance but fail to address another fundamental question, namely, Where do noise correlations, and in...
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