Posterior Parietal Cortex represents Sensory History

 

Nature volume 554, pages 368–372 (15 February 2018)

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

Athena Akrami, et.al.

Princeton Neuroscience Institute, Princeton University, Princeton, New Jersey 08544, USA

Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA

Howard Hughes Medical Institute, Princeton University, Princeton, New Jersey 08544, USA

Tactile Perception and Learning Laboratory, International School for Advanced Studies (SISSA), 34136 Trieste, Italy

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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

Finding long-term regularities in the environment, and exploiting them, is a critical brain function in a complex yet structured world. However, little is known about the neural mechanisms involved in estimating these regularities or their impact on memory. The history of sensory stimuli affects working memory and many other tasks involving sensory percepts. One salient example, discovered over a century ago and repeatedly observed in human cognition , is contraction bias, in which the representation of a stimulus held in working memory shifts towards the centre of the distribution of stimuli observed in the past (the prior distribution). Despite the ubiquity of this phenomenon, and much psychophysical and theoretical research into the use and effects of prior stimulus distributions, the neural mechanisms of contraction bias have not been identified.

On the basis of previous work using somatosensory stimuli, and inspired by parametric working memory (PWM) tasks in primates, we developed a computerized protocol to train rats, in high-throughput facilities, to perform a novel auditory PWM task. PWM tasks involve the sequential comparison of two graded (that is, analogue) stimuli separated by a delay of a few seconds. Here we used auditory pink noise stimuli; rats were rewarded for correctly reporting which of the two was louder. As with any magnitude-discrimination task, the smaller the difference between the stimuli, the harder the task. Classical contraction bias argues that during the delay, the memory of the magnitude of the memory of the early inputs drifts towards the mean of all stimuli presented.

Parametric working memory tasks, with their quantifiable behaviour, are well suited to investigating the effect of sensory history on perception and behaviour. Rodent versions of these tasks, with semi-automated training, are an efficient platform for causal and cellular-resolution investigation of neural mechanisms. By using this platform, we identified the PPC as an essential node in both the representation and causal effects of sensory-stimulus history. This represents a step towards a cellular-resolution understanding of long-standing questions about how sensory-stimulus history affects working memory and perception. Important issues that may now be addressed include how history representations in the PPC interact with current stimulus representations to modulate perception, how history information reaches the PPC, and which brain regions connected to the PPC are also essential nodes of the circuit.

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