Revealing neural correlates of behavior without behavioral measurements

Rubin, Alon; Sheintuch, Liron; Brande-Eilat, Noa; Pinchasof, Or; Rechavi, Yoav; Geva, Nitzan; Ziv, Yaniv

doi:10.1038/s41467-019-12724-2

Cited by 121 publications

(172 citation statements)

References 59 publications

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“…This motivated the subsequent quantification of single-cell selectivity to specific behaviours using shuffling analyses as well as statistical modelling with a generalized linear model (GLM). All tests indicated that PPC and M2 were driven strongly by performed behaviours, similar to what has been shown in more stereotypical tasks 27 , but extended here to freely behaving animals. The neural coding of observed behaviour, on the other hand, was below chance levels in both brain areas, even in neurons with strong performance correlates.…”

supporting

confidence: 84%

Action representation in the mouse parieto-frontal network

Tombaz

Dunn

Hovde

et al. 2020

Sci Rep

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the posterior parietal cortex (ppc) and frontal motor areas comprise a cortical network supporting goal-directed behaviour, with functions including sensorimotor transformations and decision making. in primates, this network links performed and observed actions via mirror neurons, which fire both when individuals perform an action and when they observe the same action performed by a conspecific. Mirror neurons are believed to be important for social learning, but it is not known whether mirror-like neurons occur in similar networks in other social species, such as rodents, or if they can be measured in such models using paradigms where observers passively view a demonstrator. therefore, we imaged ca 2+ responses in PPC and secondary motor cortex (M2) while mice performed and observed pellet-reaching and wheel-running tasks, and found that cell populations in both areas robustly encoded several naturalistic behaviours. However, neural responses to the same set of observed actions were absent, although we verified that observer mice were attentive to performers and that PPC neurons responded reliably to visual cues. Statistical modelling also indicated that executed actions outperformed observed actions in predicting neural responses. these results raise the possibility that sensorimotor action recognition in rodents could take place outside of the parieto-frontal circuit, and underscore that detecting socially-driven neural coding depends critically on the species and behavioural paradigm used. A key function of any motor system is the rapid and flexible production of actions in response to external stimuli, including the behaviour of other individuals. Having robust representations of performed and observed behaviours has been hypothesized to add survival value in a number of species since it could facilitate optimal action selection, gaining access to food sources or avoiding predators 1. However, which neural circuits integrate performed and observed actions, and how, are not well understood. In different species of primates and songbirds, a striking manifestation of such interactions has been described in the form of mirror neurons. Mirror neurons, first characterized in pre-motor cortex 2,3 then PPC 4 in monkeys, and later reported in humans 5 and birds 6 , respond reliably both when an individual performs a specific action and when they observe the same action performed by a conspecific. Based on these properties they have been postulated to enable specific social functions ranging from selecting appropriate actions in response to observed behaviours 2 to understanding the intentions and imitating the actions of others 7,8. After years of investigation, however, it is still debated whether mirror cells are at the basis of action understanding or if their physiological properties can be better explained by simple, temporally contingent sensory-motor associations 9. Finding mechanistic resolutions to these questions would benefit tremendously if it were possible to access cellular networks underlying social le...

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supporting

confidence: 84%

Action representation in the mouse parieto-frontal network

Tombaz

Dunn

Hovde

et al. 2020

Sci Rep

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“…This raises the question of dimensionality of the HD system during 3D motion. Previous studies 47,48 have used unsupervised approaches to reveal the 1D attractor. We did not attempt to generalize these approaches to 3D because our data is currently restricted to 60°tilt in freely moving animals, and because HD responses are largely attenuated in the rotator.…”

Section: Articlementioning

confidence: 99%

A gravity-based three-dimensional compass in the mouse brain

Angelaki

Abrego

et al. 2020

Nat Commun

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Gravity sensing provides a robust verticality signal for three-dimensional navigation. Head direction cells in the mammalian limbic system implement an allocentric neuronal compass.Here we show that head-direction cells in the rodent thalamus, retrosplenial cortex and cingulum fiber bundle are tuned to conjunctive combinations of azimuth and tilt, i.e. pitch or roll. Pitch and roll orientation tuning is anchored to gravity and independent of visual landmarks. When the head tilts, azimuth tuning is affixed to the head-horizontal plane, but also uses gravity to remain anchored to the allocentric bearings in the earth-horizontal plane. Collectively, these results demonstrate that a three-dimensional, gravity-based, neural compass is likely a ubiquitous property of mammalian species, including ground-dwelling animals.

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“…To test whether the activity in general was low-dimensional, we furthermore applied PCA directly to the deconvolved and z-scored traces of each session separately (Supplementary Figure S5B-D). Additionally, to estimate whether the activity was confined to a non-linear manifold, we calculated the internal dimensionality (Rubin et al, 2019): for a manifold of (nonlinear) dimension d, we expect the average number of neighbours within a small L2-distance r to be proportional to r d (volume of a hypersphere). To estimate d, for each point in time in each session, we found the 500 other timepoints with most similar activity (L2 distance).…”

Section: Pooled-population Activity Trajectoriesmentioning

confidence: 99%

Complete representation of action space and value in all striatal pathways

Weglage

Wärnberg

Lazaridis

et al. 2020

Preprint

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The dorsal striatum plays a central role in motor and decision programs, such as the selection and execution of particular actions and the evaluation of their outcomes. A standard circuit model has emerged based on the striatal organization where projection neurons with specific molecular and longrange connectivity identities encode discrete and possibly opposing action signals. We used large-scale cell-type specific imaging of calcium signals during motor and decision behaviors to map the activity of individual striatal projection neurons (SPNs) that form the three major output pathways of the striatum -SPNs in the D1+ direct, the A2A+ indirect, and the Oprm1+ patch pathway. We found that during exploration or choice behaviors SPNs showed a pathway-independent representation of the discrete phases and action variables. The tuning of individual SPNs was action and context-dependent, together covering the entire task space, and included pathway-independent representation of decisionvariables such as action value in a dynamic choice task. We propose that the three major SPN pathways broadcast in parallel the complete representation of the task space to downstream targets, including task-and phase-specific signals of action value and choice. The selection of specific actions is based on computations that produce prediction and evaluation of the action outcome, and correct action selection is essential for the survival of all species. Action selection computations have been associated with neuron activity in basal ganglia circuits, where the striatum plays a central role in integrating information from cortical and subcortical circuits, which is then propagated to downstream targets for action execution 1-3 . The striatum has been neuroanatomically divided into two major output pathways: the direct pathway targeting the globus pallidus interna (GPi) and the substantia nigra (SN), and the indirect pathway targeting the globus pallidus externa (GPe) 4,5 . A circuit model has emerged based on the dichotomous organization of the striatum, where the direct and indirect pathway differentially control motor programs and explain the pathophysiology of movement disorders 6-8 . In this model, the striatal pathways regulate motor behaviors through antagonistic signals. Neurochemical definitions can further divide the striatum into compartments 9,10 , for example into patch (also known as striosome) and matrix compartments where the striatal patches exhibit high levels of mu opioid receptor (MOR) expression 11,12 and form a distinct pathway that projects to the GPi and SN 13,14 . Distinct gene expression patterns can be used to genetically target and visualize the direct, indirect, and patch pathway 15-17 . Altogether, evidence from neuroanatomy and physiology have supported that the direct and indirect pathways have opposing effects on behavior. In support of this circuit model, optogenetic manipulation of the direct and indirect striatal pathways has shown their differential role in reinforcement as well as action [18][19][20]...

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Revealing neural correlates of behavior without behavioral measurements

Cited by 121 publications

References 59 publications

Action representation in the mouse parieto-frontal network

Action representation in the mouse parieto-frontal network

A gravity-based three-dimensional compass in the mouse brain

Complete representation of action space and value in all striatal pathways

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