The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

Butler, William N.; Smith, Ken G.; Meer, Matthijs A. A. van der; Taube, Jeffrey S.

doi:10.1016/j.cub.2017.03.033

Cited by 68 publications

(72 citation statements)

References 48 publications

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“…Neurons representing world-centered HD, or HD-cells, are abundant in the brain and have been studied most intensively in rodents (Cullen and Taube, 2017), but also in monkeys (Robertson et al, 1999). HD-cells reference facing direction relative to known landmarks (Taube and Burton, 1995) and are often compared to an 'internal compass' mediating our sense of direction (Butler et al, 2017;Cullen and Taube, 2017). This HD-cell compass plays a central role in cognitive mapping and is thought to mediate homing, reorientation and path integration behavior (Butler et al, 2017;Cullen and Taube, 2017;Dudchenko et al, 2019;van der Meer et al, 2010;Valerio and Taube, 2012;Weiss and Derdikman, 2018;Weiss et al, 2017).…”

Section: Visual Information and Head Directionmentioning

confidence: 99%

Behavior-dependent directional tuning in the human visual-navigation network

Nau

Schröder²,

Frey

et al. 2019

Preprint

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The brain derives cognitive maps from sensory experience to guide memory formation and behavior. Despite extensive efforts, it still remains unclear how the underlying population activity relates to active behavior and memory performance. Here, we combined 7T-fMRI with a kernelbased encoding model of virtual navigation to map world-centered directional tuning across the human cortex. First, we present an in-depth analysis of directional tuning in visual, retrosplenial and parahippocampal cortices and the hippocampus. Second, we show that tuning strength, width and topology of this directional code during memory-guided navigation depend on successful encoding of the environment. Finally, we show that participants' locomotory state influences this tuning in sensory and mnemonic regions such as the hippocampus. We demonstrate a direct link between neural population tuning and human cognition and show that high-level memory processing interacts with network-wide environmental coding in the service of behavior.

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Section: Visual Information and Head Directionmentioning

confidence: 99%

Behavior-dependent directional tuning in the human visual-navigation network

Nau

Schröder²,

Frey

et al. 2019

Preprint

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“…Recurrent loops with offsets move the activity 'bump' around the ring as the animal turns ( Figure 1B-D), and the compass-like representation is tethered to the animal's surroundings through visual inputs, which are used as a reference to guide heading ( Figure 1E,F). Experimental support for this general theoretical formulation has come from analyses of head-direction cell population activity under a variety of different conditions (Butler et al, 2017;Chaudhuri et al, 2019;Clark and Taube, 2012;Hargreaves et al, 2007;Muir et al, 2009;Peyrache et al, 2015;Taube et al, 1990b;Yoganarasimha et al, 2006). However, different ring attractor networks make distinct assumptions about the connectivities of their constituent neurons (Ben-Yishai et al, 1995;Xie et al, 2002;Zhang, 1996) (for example, Figure 1A-F).…”

Section: Introductionmentioning

confidence: 99%

“…This internal representation likely guides navigation behaviors. Indeed, perturbations to the system in rats induce errors in path-integration (Butler et al, 2017;Valerio and Taube, 2012). A large body of theoretical work has addressed conceptual questions about how this representation of head direction is generated and updated (Knierim and Zhang, 2012).…”

Section: Introductionmentioning

confidence: 99%

The neuroanatomical ultrastructure and function of a biological ring attractor

Turner-Evans

Jensen

Ali

et al. 2019

Preprint

105

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Neural representations of head direction have been discovered in many different species. A large body of theoretical work has proposed that the dynamics associated with these representations might be generated, maintained, and updated by recurrent network structures called ring attractors. Ring attractor models rely on specific assumptions about the structure of excitatory and inhibitory connectivity. These assumptions have been difficult to test directly. We therefore performed electron-microscopy-based circuit reconstruction and RNA profiling of identified cell types in the heading direction system of Drosophila melanogaster to directly examine excitatory and inhibitory synaptic connectivity, generating a dataset that should serve as a reference for future functional studies of the network. Consistent with several theoretical models, we identified network motifs that have been hypothesized to maintain the heading representation in darkness, update it when the animal turns, and tether it to visual cues. Genetically targeted two-photon calcium imaging and thermogenetic perturbation of the constituent neuron types during behavior provided additional support for these functional roles. However, we also discovered network motifs absent in current models, including a surprising degree of recurrence between arbors of different neurons with mixed pre-and post-synaptic specializations. Overall, our results confirm that the Drosophila heading direction network contains the core components of a ring attractor while also revealing unpredicted structural features that might enable the heading system to accurately track the animal's heading with a small number of neurons. Importantly, however, these and other models of attractor networks in the fly have assumed the circuit's connectivity based on relatively indirect evidence (Cope et al., 2017;Han et al., 2019;Kakaria and de Bivort, 2017;Kim et al., 2017;Su et al., 2017;Turner-Evans et al., 2017). For example, the location of pre-and post-synaptic arbors has been inferred from whether neural processes visible in light-microscopic images seem spine-or bouton-like in specific substructures (Hanesch et al., 1989;Lin et al., 2013;Wolff et al., 2015). The hypothesized connectivity of the circuit has then been derived from light-level overlap between the putatively pre-and post-synaptic arbors of neurons . In Drosophila, such conclusions have been bolstered by employing GFP-reconstitution-acrosssynaptic-partners (GRASP) (Xie et al., 2017) and trans-Tango (Omoto et al., 2018) techniques. Although both GRASP and trans-Tango are powerful techniques, their reliability and accuracy when used to estimate pairwise connectivity is limited (Lee et al., 2017; Talay et al., 2017). Similarly, measurements of functional connectivity by optogenetic stimulation of one neuron type and calcium imaging of another (Franconville et al., 2018) cannot conclusively establish the presence or absence of monosynaptic connectivity.In the current study, we established the synaptic-and cellular-resolution str...

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“…Very little is known about how Drosophila – or any species – use heading signals to guide navigational behavior [47,48]. Behavioral experiments have argued that flies can navigate to remembered 2D locations in space [41,49].…”

Section: From Heading Signals To Behaviormentioning

confidence: 99%

Building a heading signal from anatomically defined neuron types in the Drosophila central complex

Green

Maimon

2018

Current Opinion in Neurobiology

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A network of a few hundred neurons in the Drosophila central complex carries an estimate of the fly's heading in the world, akin to the mammalian head-direction system. Here we describe how anatomically defined neuronal classes in this network are poised to implement specific sub-processes for building and updating this population-level heading signal. The computations we describe in the fly central complex strongly resemble those posited to exist in the mammalian brain, in computational models for building head-direction signals. By linking circuit anatomy to navigational physiology, the Drosophila central complex should provide a detailed example of how a heading signal is built.

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The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

Cited by 68 publications

References 48 publications

Behavior-dependent directional tuning in the human visual-navigation network

Behavior-dependent directional tuning in the human visual-navigation network

The neuroanatomical ultrastructure and function of a biological ring attractor

Building a heading signal from anatomically defined neuron types in the Drosophila central complex

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