Intracellular dynamics of hippocampal place cells during virtual navigation

Harvey, Christopher D.; Collman, Forrest; Dombeck, Daniel A.; Tank, David W.

doi:10.1038/nature08499

Cited by 826 publications

(1,011 citation statements)

References 42 publications

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“…Studies have used visually stimuli in the upper visual field which require approach behaviors (Harvey, Collman, Dombeck, & Tank, 2009; Scott, Constantinople, Erlich, Tank, & Brody, 2015). Conversely, other studies have employed stimuli which occur in the lower visual field, and which require avoidance behaviors (Ho et al, 2015; Manita et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Segregated fronto‐cortical and midbrain connections in the mouse and their relation to approach and avoidance orienting behaviors

Savage

McQuade

Thiele

2017

J of Comparative Neurology

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The orchestration of orienting behaviors requires the interaction of many cortical and subcortical areas, for example the superior colliculus (SC), as well as prefrontal areas responsible for top–down control. Orienting involves different behaviors, such as approach and avoidance. In the rat, these behaviors are at least partially mapped onto different SC subdomains, the lateral (SCl) and medial (SCm), respectively. To delineate the circuitry involved in the two types of orienting behavior in mice, we injected retrograde tracer into the intermediate and deep layers of the SCm and SCl, and thereby determined the main input structures to these subdomains. Overall the SCm receives larger numbers of afferents compared to the SCl. The prefrontal cingulate area (Cg), visual, oculomotor, and auditory areas provide strong input to the SCm, while prefrontal motor area 2 (M2), and somatosensory areas provide strong input to the SCl. The prefrontal areas Cg and M2 in turn connect to different cortical and subcortical areas, as determined by anterograde tract tracing. Even though connectivity pattern often overlap, our labeling approaches identified segregated neural circuits involving SCm, Cg, secondary visual cortices, auditory areas, and the dysgranular retrospenial cortex likely to be involved in avoidance behaviors. Conversely, SCl, M2, somatosensory cortex, and the granular retrospenial cortex comprise a network likely involved in approach/appetitive behaviors.

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Section: Discussionmentioning

confidence: 99%

Segregated fronto‐cortical and midbrain connections in the mouse and their relation to approach and avoidance orienting behaviors

Savage

McQuade

Thiele

2017

J of Comparative Neurology

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“…We used a modified version of the visual virtual reality system that has been described previously 31 . Head-restrained mice ran on a spherical treadmill.…”

Section: Methodsmentioning

confidence: 99%

Distinct timescales of population coding across cortex

Runyan

Piasini

Panzeri

et al. 2017

Nature

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345

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The cortex represents information across widely varying timescales1–5. For instance, sensory cortex encodes stimuli that fluctuate over few tens of milliseconds6,7, whereas in association cortex behavioral choices can require the maintenance of information over seconds8,9. However, it remains poorly understood if diverse timescales result mostly from features intrinsic to individual neurons or from neuronal population activity. This question is unanswered because the timescales of coding in populations of neurons have not been studied extensively, and population codes have not been compared systematically across cortical regions. Here we discovered that population codes can be essential to achieve long coding timescales. Furthermore, we found that the properties of population codes differ between sensory and association cortices. We compared coding for sensory stimuli and behavioral choices in auditory cortex (AC) and posterior parietal cortex (PPC) as mice performed a sound localization task. Auditory stimulus information was stronger in AC than in PPC, and both regions contained choice information. Although AC and PPC coded information by tiling in time neurons that were transiently informative for ~200 milliseconds, the areas had major differences in functional coupling between neurons, measured as activity correlations that could not be explained by task events. Coupling among PPC neurons was strong and extended over long time lags, whereas coupling among AC neurons was weak and short-lived. Stronger coupling in PPC led to a population code with long timescales and a representation of choice that remained consistent for approximately one second. In contrast, AC had a code with rapid fluctuations in stimulus and choice information over hundreds of milliseconds. Our results reveal that population codes differ across cortex and that coupling is a variable property of cortical populations that affects the timescale of information coding and the accuracy of behavior.

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“…We also analyzed recordings of 14 CA1 pyramidal cells (n=4 labeled) during different behaviors. Some of these neurons fired as place cells [28][29][30] during spatial navigation and we tested some of their molecular expression patterns ( Fig. 3 and Table 1).…”

Section: Identification Of Neurons Recorded In Freely-moving Ratsmentioning

confidence: 99%

Behavior-dependent specialization of identified hippocampal interneurons

et al. 2012

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A large variety of GABAergic interneurons control information processing in hippocampal circuits governing the formation of neuronal representations. Whether distinct hippocampal interneuron types contribute differentially to information-processing during behavior is not known. We employed a novel technique for recording and labeling interneurons and pyramidal cells in drug-free, freely-moving rats. Recorded parvalbumin-expressing basket interneurons innervate somata and proximal pyramidal cell dendrites, whereas nitric-oxide-synthase-and neuropeptide-Y-expressing ivy cells provide synaptic and extrasynaptic dendritic modulation. Basket and ivy cells showed distinct spike timing dynamics, firing at different rates and times during theta and ripple oscillations. Basket but not ivy cells changed their firing rates during movement, sleep and quiet wakefulness, suggesting that basket cells coordinate cell assemblies in a behavioral state-contingent manner, whereas persistently-firing ivy cells might control network excitability and homeostasis. Different interneuron types provide GABA to specific subcellular domains at defined times and rates, thus differentially controlling network activity during behavior.GABAergic interneurons control information processing in cortical circuits as percussionists set the rhythm for a melody, or traffic lights regulate the movement of cars through a city. Interneurons generate oscillatory activity 1, 2 , synchronize the activity of pyramidal cells 3 and set time windows for synaptic integration 4 . A large diversity of interneuronal types is a hallmark of cortical circuits. Different domains of pyramidal cells, such as the soma, axoninitial-segment, proximal or distal dendrites 5 are innervated by distinct types of GABAergic interneuron. They also have distinct inputs and membrane properties 6-10 and show different firing patterns during network oscillations induced in vitro [11][12][13][14] or recorded in anesthetized animals 15 , indicating distinct roles for specific interneuron types. However, research on interneurons in drug-free animals that can freely change their behavior, has so far been limited to recordings from unidentified interneurons because of technical limitations. In the barrel cortex of head-restrained mice, groups of interneurons with distinct membrane dynamics during different behavioral states have been described 16,17 and in the hippocampus unidentified interneurons or interneurons belonging to heterogeneous groups expressing parvalbumin and/or somatostatin have been reported [18][19][20][21] to fire with different firing patterns during network oscillations. But, how do specific types of identified interneurons control the activity of cortical circuits in freely-moving animals? CouldCorrespondence and requests for materials should be addressed to D.L. (damien.lapray@pharm.ox.ac.uk) Results Identification of neurons recorded in freely-moving ratsWe recorded the activity of parvalbumin (PV)-expressing basket, ivy and pyramidal cells in the dorsal CA...

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Intracellular dynamics of hippocampal place cells during virtual navigation

Cited by 826 publications

References 42 publications

Segregated fronto‐cortical and midbrain connections in the mouse and their relation to approach and avoidance orienting behaviors

Segregated fronto‐cortical and midbrain connections in the mouse and their relation to approach and avoidance orienting behaviors

Distinct timescales of population coding across cortex

Behavior-dependent specialization of identified hippocampal interneurons

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