Title: Response sub-additivity and variability quenching in visual cortex
Sub-additivity and variability are ubiquitous response motifs in primary visual cortex (V1). Response sub-additivity provides a sign of the brain processes that enable us to construct useful interpretations of the visual environment (i.e., nonlinear input transformations), while response variability provides a sign of the brain processes that limit the precision with which we can do this (i.e., neural information loss). Historically, these two motifs have been studied independently of each other. Yet, there is increasing evidence that experimen- tal manipulations that elicit response sub-additivity often also quench response variability. Here we provide a unifying review of these phenomena, suggesting that response sub-additivity and variability quenching may have a common origin. We review empirical findings as well as recent model-based insights into the functional operations, computational objectives, and circuit mechanisms underlying V1 activity. Although these model- ing approaches address different aspects of cortical activity, they all predict that response sub-additivity and variability quenching will often co-occur. Response sub-additivity and variability quenching are not limited to V1 but are widespread cortical phenomena. Many of the insights we review generalize to other cortical areas, suggesting that the connection between response sub-additivity and variability quenching may be a canonical motif across cortex. more »« less
Froudarakis, Emmanouil; Fahey, Paul G.; Reimer, Jacob; Smirnakis, Stelios M.; Tehovnik, Edward J.; Tolias, Andreas S.
(, Annual Review of Vision Science)
null
(Ed.)
In this article, we review the anatomical inputs and outputs to the mouse primary visual cortex, area V1. Our survey of data from the Allen Institute Mouse Connectivity project indicates that mouse V1 is highly interconnected with both cortical and subcortical brain areas. This pattern of innervation allows for computations that depend on the state of the animal and on behavioral goals, which contrasts with simple feedforward, hierarchical models of visual processing. Thus, to have an accurate description of the function of V1 during mouse behavior, its involvement with the rest of the brain circuitry has to be considered. Finally, it remains an open question whether the primary visual cortex of higher mammals displays the same degree of sensorimotor integration in the early visual system.
Liska, John P; Rowley, Declan P; Nguyen, Trevor_Thai Kim; Muthmann, Jens-Oliver; Butts, Daniel A; Yates, Jacob; Huk, Alexander C
(, eLife)
When mice run, activity in their primary visual cortex (V1) is strongly modulated. This observation has altered conceptions of a brain region assumed to be a passive image processor. Extensive work has followed to dissect the circuits and functions of running-correlated modulation. However, it remains unclear whether visual processing in primates might similarly change during locomotion. We therefore measured V1 activity in marmosets while they viewed stimuli on a treadmill. In contrast to mouse, running-correlated modulations of marmoset V1 were small and tended to be slightly suppressive. Population-level analyses revealed trial-to-trial fluctuations of shared gain across V1 in both species, but while strongly correlated with running in mice, gain modulations were smaller and more often negatively correlated with running in marmosets. Thus, population-wide fluctuations of V1 may reflect a common feature of mammalian visual cortical function, but important quantitative differences point to distinct consequences for the relation between vision and action in primates versus rodents.
Powell, Nathaniel J; Hein, Bettina; Kong, Deyue; Elpelt, Jonas; Mulholland, Haleigh N; Kaschube, Matthias; Smith, Gordon B
(, Proceedings of the National Academy of Sciences)
In order to deal with a complex environment, animals form a diverse range of neural representations that vary across cortical areas, ranging from largely unimodal sensory input to higher-order representations of goals, outcomes, and motivation. The developmental origin of this diversity is currently unclear, as representations could arise through processes that are already area-specific from the earliest developmental stages or alternatively, they could emerge from an initially common functional organization shared across areas. Here, we use spontaneous activity recorded with two-photon and widefield calcium imaging to reveal the functional organization across the early developing cortex in ferrets, a species with a well-characterized columnar organization and modular structure of spontaneous activity in the visual cortex. We find that in animals 7 to 14 d prior to eye-opening and ear canal opening, spontaneous activity in both sensory areas (auditory and somatosensory cortex, A1 and S1, respectively), and association areas (posterior parietal and prefrontal cortex, PPC and PFC, respectively) showed an organized and modular structure that is highly similar to the organization in V1. In all cortical areas, this modular activity was distributed across the cortical surface, forming functional networks that exhibit millimeter-scale correlations. Moreover, this modular structure was evident in highly coherent spontaneous activity at the cellular level, with strong correlations among local populations of neurons apparent in all cortical areas examined. Together, our results demonstrate a common distributed and modular organization across the cortex during early development, suggesting that diverse cortical representations develop initially according to similar design principles.
Abstract The recent publications of the inter-areal connectomes for mouse, marmoset, and macaque cortex have allowed deeper comparisons across rodent vs. primate cortical organization. In general, these show that the mouse has very widespread, “all-to-all” inter-areal connectivity (i.e. a “highly dense” connectome in a graph theoretical framework), while primates have a more modular organization. In this review, we highlight the relevance of these differences to function, including the example of primary visual cortex (V1) which, in the mouse, is interconnected with all other areas, therefore including other primary sensory and frontal areas. We argue that this dense inter-areal connectivity benefits multimodal associations, at the cost of reduced functional segregation. Conversely, primates have expanded cortices with a modular connectivity structure, where V1 is almost exclusively interconnected with other visual cortices, themselves organized in relatively segregated streams, and hierarchically higher cortical areas such as prefrontal cortex provide top–down regulation for specifying precise information for working memory storage and manipulation. Increased complexity in cytoarchitecture, connectivity, dendritic spine density, and receptor expression additionally reveal a sharper hierarchical organization in primate cortex. Together, we argue that these primate specializations permit separable deconstruction and selective reconstruction of representations, which is essential to higher cognition.
Xia, Ji; Marks, Tyler D.; Goard, Michael J.; Wessel, Ralf
(, Journal of Neurophysiology)
null
(Ed.)
Both experimenter-controlled stimuli and stimulus-independent variables impact cortical neural activity. A major hurdle to understanding neural representation is distinguishing between qualitatively different causes of the fluctuating population activity. We applied an unsupervised low-rank tensor decomposition analysis to the recorded population activity in the visual cortex of awake mice in response to repeated presentations of naturalistic visual stimuli. We found that neurons covaried largely independently of individual neuron stimulus response reliability and thus encoded both stimulus-driven and stimulus-independent variables. Importantly, a neuron’s response reliability and the neuronal coactivation patterns substantially reorganized for different external visual inputs. Analysis of recurrent balanced neural network models revealed that both the stimulus specificity and the mixed encoding of qualitatively different variables can arise from clustered external inputs. These results establish that coactive neurons with diverse response reliability mediate a mixed representation of stimulus-driven and stimulus-independent variables in the visual cortex. NEW & NOTEWORTHY V1 neurons covary largely independently of individual neuron’s response reliability. A single neuron’s response reliability imposes only a weak constraint on its encoding capabilities. Visual stimulus instructs a neuron’s reliability and coactivation pattern. Network models revealed using clustered external inputs.
@article{osti_10519395,
place = {Country unknown/Code not available},
title = {Response sub-additivity and variability quenching in visual cortex},
url = {https://par.nsf.gov/biblio/10519395},
DOI = {10.1038/s41583-024-00795-0},
abstractNote = {Sub-additivity and variability are ubiquitous response motifs in primary visual cortex (V1). Response sub-additivity provides a sign of the brain processes that enable us to construct useful interpretations of the visual environment (i.e., nonlinear input transformations), while response variability provides a sign of the brain processes that limit the precision with which we can do this (i.e., neural information loss). Historically, these two motifs have been studied independently of each other. Yet, there is increasing evidence that experimen- tal manipulations that elicit response sub-additivity often also quench response variability. Here we provide a unifying review of these phenomena, suggesting that response sub-additivity and variability quenching may have a common origin. We review empirical findings as well as recent model-based insights into the functional operations, computational objectives, and circuit mechanisms underlying V1 activity. Although these model- ing approaches address different aspects of cortical activity, they all predict that response sub-additivity and variability quenching will often co-occur. Response sub-additivity and variability quenching are not limited to V1 but are widespread cortical phenomena. Many of the insights we review generalize to other cortical areas, suggesting that the connection between response sub-additivity and variability quenching may be a canonical motif across cortex.},
journal = {Nature Reviews Neuroscience},
volume = {25},
number = {4},
publisher = {Nature Portfolio},
author = {Goris, Robbe_L T and Coen-Cagli, Ruben and Miller, Kenneth D and Priebe, Nicholas J and Lengyel, Máté},
}
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