Attention:The NSF Public Access Repository (PAR) system and access will be unavailable from 11:00 PM ET on Thursday, October 15th until 12:00 AM ET on Friday, October 16th due to maintenance. We apologize for the inconvenience.


Title: Scaling of sensory information in large neural populations shows signatures of information-limiting correlations
Abstract How is information distributed across large neuronal populations within a given brain area? Information may be distributed roughly evenly across neuronal populations, so that total information scales linearly with the number of recorded neurons. Alternatively, the neural code might be highly redundant, meaning that total information saturates. Here we investigate how sensory information about the direction of a moving visual stimulus is distributed across hundreds of simultaneously recorded neurons in mouse primary visual cortex. We show that information scales sublinearly due to correlated noise in these populations. We compartmentalized noise correlations into information-limiting and nonlimiting components, then extrapolate to predict how information grows with even larger neural populations. We predict that tens of thousands of neurons encode 95% of the information about visual stimulus direction, much less than the number of neurons in primary visual cortex. These findings suggest that the brain uses a widely distributed, but nonetheless redundant code that supports recovering most sensory information from smaller subpopulations.  more » « less
Award ID(s):
1707398
PAR ID:
10247739
Author(s) / Creator(s):
; ; ; ; ; ; ;
Date Published:
Journal Name:
Nature Communications
Volume:
12
Issue:
1
ISSN:
2041-1723
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Sensory data about most natural task-relevant variables are entangled with task-irrelevant nuisance variables. The neurons that encode these relevant signals typically constitute a nonlinear population code. Here we present a theoretical framework for quantifying how the brain uses or decodes its nonlinear information. Our theory obeys fundamental mathematical limitations on information content inherited from the sensory periphery, describing redundant codes when there are many more cortical neurons than primary sensory neurons. The theory predicts that if the brain uses its nonlinear population codes optimally, then more informative patterns should be more correlated with choices. More specifically, the theory predicts a simple, easily computed quantitative relationship between fluctuating neural activity and behavioral choices that reveals the decoding efficiency. This relationship holds for optimal feedforward networks of modest complexity, when experiments are performed under natural nuisance variation. We analyze recordings from primary visual cortex of monkeys discriminating the distribution from which oriented stimuli were drawn, and find these data are consistent with the hypothesis of near-optimal nonlinear decoding. 
    more » « less
  2. The retina and primary visual cortex (V1) both exhibit diverse neural populations sensitive to diverse visual features. Yet it remains unclear how neural populations in each area partition stimulus space to span these features. One possibility is that neural populations are organized into discrete groups of neurons, with each group signaling a particular constellation of features. Alternatively, neurons could be continuously distributed across feature-encoding space. To distinguish these possibilities, we presented a battery of visual stimuli to the mouse retina and V1 while measuring neural responses with multi-electrode arrays. Using machine learning approaches, we developed a manifold embedding technique that captures how neural populations partition feature space and how visual responses correlate with physiological and anatomical properties of individual neurons. We show that retinal populations discretely encode features, while V1 populations provide a more continuous representation. Applying the same analysis approach to convolutional neural networks that model visual processing, we demonstrate that they partition features much more similarly to the retina, indicating they are more like big retinas than little brains. 
    more » « less
  3. Flexibly responding to sensory cues is fundamental to animal behavior. However, growing evidence suggests that the relevant neural circuits have been incompletely resolved. We investigated the midbrain reticular formation's (MRF) role, training mice to apply an abstract rule mapping identical visual stimuli to opposing actions across contexts. Large-scale recordings revealed that neurons in MRF, along with several canonical decision-making areas, maintained persistent representations of task context in pre-stimulus activity. These representations predicted divergent population dynamics, putatively routing stimuli toward context-appropriate actions. The MRF was the only recorded region containing neuronal populations that both predicted lapses in contextual control pre-stimulus and exhibited contextually modulated premotor responses. The MRF also showed task-specific sensory plasticity. Context-coding neurons were aligned with cortical inputs, suggesting spatial organization. These findings support the hypothesis that the MRF is a key node for setting and implementing abstract contextual states within the distributed circuitry for flexible perceptual decisions. 
    more » « less
  4. Klann, Eric (Ed.)
    Abstract As information about the world is conveyed from the sensory periphery to central neural circuits, it mixes with complex ongoing cortical activity. How do neural populations keep track of sensory signals, separating them from noisy ongoing activity? Here, we show that sensory signals are encoded more reliably in certain low-dimensional subspaces. These coding subspaces are defined by correlations between neural activity in the primary sensory cortex and upstream sensory brain regions; the most correlated dimensions were best for decoding. We analytically show that these correlation-based coding subspaces improve, reaching optimal limits (without an ideal observer), as noise correlations between cortex and upstream regions are reduced. We show that this principle generalizes across diverse sensory stimuli in the olfactory system and the visual system of awake mice. Our results demonstrate an algorithm the cortex may use to multiplex different functions, processing sensory input in low-dimensional subspaces separate from other ongoing functions. 
    more » « less
  5. Abstract Traumatic brain injury (TBI) affects neural function at the local injury site and also at distant, connected brain areas. However, the real‐time neural dynamics in response to injury and subsequent effects on sensory processing and behaviour are not fully resolved, especially across a range of spatial scales. We used in vivo calcium imaging in awake, head‐restrained male and female mice to measure large‐scale and cellular resolution neuronal activation, respectively, in response to a mild/moderate TBI induced by focal controlled cortical impact (CCI) injury of the motor cortex (M1). Widefield imaging revealed an immediate CCI‐induced activation at the injury site, followed by a massive slow wave of calcium signal activation that travelled across the majority of the dorsal cortex within approximately 30 s. Correspondingly, two‐photon calcium imaging in the primary somatosensory cortex (S1) found strong activation of neuropil and neuronal populations during the CCI‐induced travelling wave. A depression of calcium signals followed the wave, during which we observed the atypical activity of a sparse population of S1 neurons. Longitudinal imaging in the hours and days after CCI revealed increases in the area of whisker‐evoked sensory maps at early time points, in parallel to decreases in cortical functional connectivity and behavioural measures. Neural and behavioural changes mostly recovered over hours to days in our M1‐TBI model, with a more lasting decrease in the number of active S1 neurons. Our results in unanaesthetized mice describe novel spatial and temporal neural adaptations that occur at cortical sites remote to a focal brain injury. 
    more » « less