scholarly journals Functional and anatomical relationships between the medial precentral cortex, dorsal striatum, and head direction cell circuitry. II. Neuroanatomical studies

2019 ◽  
Vol 121 (2) ◽  
pp. 371-395 ◽  
Author(s):  
Max L. Mehlman ◽  
Shawn S. Winter ◽  
Jeffrey S. Taube
Keyword(s):  
Limbic System ◽  
Dorsal Striatum ◽  
Cell Types ◽  
Spatial Processing ◽  
Small Populations ◽  
Head Direction ◽  
Functional Relationships ◽  
Anatomical Basis ◽  
Direct Input ◽  
Self Motion

An animal’s directional heading within its environment is encoded by the activity of head direction (HD) cells. In rodents, these neurons are found primarily within the limbic system in the interconnected structures that form the limbic HD circuit. In our accompanying report in this issue, we describe two HD cell populations located outside of this circuit in the medial precentral cortex (PrCM) and dorsal striatum (DS). These extralimbic areas receive their HD signals from the limbic system but do not provide critical input or feedback to limbic HD cells (Mehlman ML, Winter SS, Valerio S, Taube JS. J Neurophysiol 121: 350–370, 2019.). In this report, we complement our previous lesion and recording experiments with a series of neuroanatomical tracing studies in rats designed to examine patterns of connectivity between the PrCM, DS, limbic HD circuit, and related spatial processing circuitry. Retrograde tracing revealed that the DS receives direct input from numerous structures known to contain HD cells and/or other spatially tuned cell types. Importantly, these projections preferentially target and converge within the most medial portion of the DS, the same area in which we previously recorded HD cells. The PrCM receives direct input from a subset of these spatial processing structures. Anterograde tracing identified indirect pathways that could permit the PrCM and DS to convey self-motion information to the limbic HD circuit. These tracing studies reveal the anatomical basis for the functional relationships observed in our lesion and recording experiments. Collectively, these findings expand our understanding of how spatial processing circuitry functionally and anatomically extends beyond the limbic system into the PrCM and DS. NEW & NOTEWORTHY Head direction (HD) cells are located primarily within the limbic system, but small populations of extralimbic HD cells are found in the medial precentral cortex (PrCM) and dorsal striatum (DS). The neuroanatomical tracing experiments reported here explored the pathways capable of transmitting the HD signal to these extralimbic areas. We found that projections arising from numerous spatial processing structures converge within portions of the PrCM and DS that contain HD cells.

scholarly journals Functional and anatomical relationships between the medial precentral cortex, dorsal striatum, and head direction cell circuitry. I. Recording studies

2019 ◽  
Vol 121 (2) ◽  
pp. 350-370 ◽  
Author(s):  
Max L. Mehlman ◽  
Shawn S. Winter ◽  
Stephane Valerio ◽  
Jeffrey S. Taube
Keyword(s):  
Limbic System ◽  
Functional Relationship ◽  
Thalamic Nucleus ◽  
Cell Activity ◽  
Dorsal Striatum ◽  
Small Populations ◽  
Head Direction ◽  
Sense Of Direction ◽  
Combined Lesions ◽  
Self Motion

Head direction (HD) cells fire as a function of the animal’s directional heading and provide the animal with a sense of direction. In rodents, these neurons are located primarily within the limbic system, but small populations of HD cells are found in two extralimbic areas: the medial precentral cortex (PrCM) and dorsal striatum (DS). HD cell activity in these structures could be driven by output from the limbic HD circuit or generated intrinsically. We examined these possibilities by recording the activity of PrCM and DS neurons in control rats and in rats with anterodorsal thalamic nucleus (ADN) lesions, a manipulation that disrupts the limbic HD signal. HD cells in the PrCM and DS of control animals displayed characteristics similar to those of limbic HD cells, and these extralimbic HD signals were eliminated in animals with complete ADN lesions, suggesting that the PrCM and DS HD signals are conveyed from the limbic HD circuit. Angular head velocity cells recorded in the PrCM and DS were unaffected by ADN lesions. Next, we determined if the PrCM and DS convey necessary self-motion signals to the limbic HD circuit. Limbic HD cell activity recorded in the ADN remained intact following combined lesions of the PrCM and DS. Collectively, these experiments reveal a unidirectional functional relationship between the limbic HD circuit and the PrCM and DS; the limbic system generates the HD signal and transmits it to the PrCM and DS, but these extralimbic areas do not provide critical input or feedback to limbic HD cells. NEW & NOTEWORTHY Head direction (HD) cells have been extensively studied within the limbic system. The lesion and recording experiments reported here examined two relatively understudied populations of HD cells located outside of the canonical limbic HD circuit in the medial precentral cortex and dorsal striatum. We found that HD cell activity in these two extralimbic areas is driven by output from the limbic HD circuit, revealing that HD cell circuitry functionally extends beyond the limbic system.

scholarly journals Active Locomotion Increases Peak Firing Rates of Anterodorsal Thalamic Head Direction Cells

2001 ◽  
Vol 86 (2) ◽  
pp. 692-702 ◽  
Author(s):  
Michaël B. Zugaro ◽  
Eiichi Tabuchi ◽  
Céline Fouquier ◽  
Alain Berthoz ◽  
Sidney I. Wiener
Keyword(s):  
Visual Cues ◽  
Head Direction ◽  
Small Reservoir ◽  
Motion Cues ◽  
Preferred Direction ◽  
State Dependent ◽  
Command Signals ◽  
Rats And Mice ◽  
Foraging Task ◽  
Self Motion

Head direction (HD) cells discharge selectively in macaques, rats, and mice when they orient their head in a specific (“preferred”) direction. Preferred directions are influenced by visual cues as well as idiothetic self-motion cues derived from vestibular, proprioceptive, motor efferent copy, and command signals. To distinguish the relative importance of active locomotor signals, we compared HD cell response properties in 49 anterodorsal thalamic HD cells of six male Long-Evans rats during active displacements in a foraging task as well as during passive rotations. Since thalamic HD cells typically stop firing if the animals are tightly restrained, the rats were trained to remain immobile while drinking water distributed at intervals from a small reservoir at the center of a rotatable platform. The platform was rotated in a clockwise/counterclockwise oscillation to record directional responses in the stationary animals while the surrounding environmental cues remained stable. The peak rate of directional firing decreased by 27% on average during passive rotations ( r 2 = 0.73, P< 0.001). Individual cells recorded in sequential sessions ( n = 8) reliably showed comparable reductions in peak firing, but simultaneously recorded cells did not necessarily produce identical responses. All of the HD cells maintained the same preferred directions during passive rotations. These results are consistent with the hypothesis that the level of locomotor activity provides a state-dependent modulation of the response magnitude of AD HD cells. This could result from diffusely projecting neuromodulatory systems associated with motor state.

scholarly journals Nucleus reuniens of the thalamus contains head direction cells

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Maciej M Jankowski ◽  
Md Nurul Islam ◽  
Nicholas F Wright ◽  
Seralynne D Vann ◽  
Jonathan T Erichsen ◽  
...  
Keyword(s):  
Spatial Processing ◽  
Brain Cells ◽  
Head Direction ◽  
Head Direction Cells ◽  
Nucleus Reuniens ◽  
Connected Network ◽  
Heading Direction ◽  
Freely Moving ◽  
First Time ◽  
Discrete Populations

Discrete populations of brain cells signal heading direction, rather like a compass. These ‘head direction’ cells are largely confined to a closely-connected network of sites. We describe, for the first time, a population of head direction cells in nucleus reuniens of the thalamus in the freely-moving rat. This novel subcortical head direction signal potentially modulates the hippocampal CA fields directly and, thus, informs spatial processing and memory.

scholarly journals Functional connectivity of the entorhinal–hippocampal space circuit

2014 ◽  
Vol 369 (1635) ◽  
pp. 20120516 ◽  
Author(s):  
Sheng-Jia Zhang ◽  
Jing Ye ◽  
Jonathan J. Couey ◽  
Menno Witter ◽  
Edvard I. Moser ◽  
...  
Keyword(s):  
Entorhinal Cortex ◽  
Cell Types ◽  
Place Cells ◽  
Projection Neurons ◽  
Border Cells ◽  
Head Direction ◽  
Grid Cells ◽  
Head Direction Cells ◽  
Dynamic Interactions ◽  
Cell Groups

The mammalian space circuit is known to contain several functionally specialized cell types, such as place cells in the hippocampus and grid cells, head-direction cells and border cells in the medial entorhinal cortex (MEC). The interaction between the entorhinal and hippocampal spatial representations is poorly understood, however. We have developed an optogenetic strategy to identify functionally defined cell types in the MEC that project directly to the hippocampus. By expressing channelrhodopsin-2 (ChR2) selectively in the hippocampus-projecting subset of entorhinal projection neurons, we were able to use light-evoked discharge as an instrument to determine whether specific entorhinal cell groups—such as grid cells, border cells and head-direction cells—have direct hippocampal projections. Photoinduced firing was observed at fixed minimal latencies in all functional cell categories, with grid cells as the most abundant hippocampus-projecting spatial cell type. We discuss how photoexcitation experiments can be used to distinguish the subset of hippocampus-projecting entorhinal neurons from neurons that are activated indirectly through the network. The functional breadth of entorhinal input implied by this analysis opens up the potential for rich dynamic interactions between place cells in the hippocampus and different functional cell types in the entorhinal cortex (EC).

Specific binding of [3H]oxytocin in the female rat brain

1983 ◽  
Vol 61 (9) ◽  
pp. 989-995 ◽  
Author(s):  
B. M. Ferrier ◽  
S.A. McClorry ◽  
A. W. Cochrane
Keyword(s):  
Plasma Membrane ◽  
Limbic System ◽  
Microsomal Fraction ◽  
Specific Binding ◽  
Cell Types ◽  
Time Dependent ◽  
Female Rat ◽  
Ph Optimum ◽  
Rat Tissue ◽  
Different Cell Types

Because of demonstrated effects of oxytocin on some limbic system mediated behaviours, the specific binding of [3H]oxytocin to a plasma membrane containing fraction of rat limbic tissue has been studied. The binding of the microsomal fraction of estrogenized, female rat tissue was time dependent and saturable, with a Bmax of 2.5 × 10−l3 moles per milligram of protein and an apparent KD of 3.53 × 10−8 M, and appeared to show positive cooperativity. The pH optimum of the binding was 6.0, close to the pH optimum for oxytocin – neurophysin binding; however, other results show the two types of binding to be different. The microsomal fraction did not appreciably degrade oxytocin under the conditions used for [3H]oxytocin binding. The distribution in limbic tissue of oxytocin-degrading activity and of individual enzymes capable of degrading oxytocin has been examined and an interplay of enzymes concentrated in different cell types is proposed.

scholarly journals Both visual and idiothetic cues contribute to head direction cell stability during navigation along complex routes

2011 ◽  
Vol 105 (6) ◽  
pp. 2989-3001 ◽  
Author(s):  
Ryan M. Yoder ◽  
Benjamin J. Clark ◽  
Joel E. Brown ◽  
Mignon V. Lamia ◽  
Stephane Valerio ◽  
...  
Keyword(s):  
Visual Information ◽  
Path Integration ◽  
Visual Cues ◽  
Cell Activity ◽  
Neural Representation ◽  
Head Direction ◽  
Motion Cues ◽  
Cell Stability ◽  
Self Motion ◽  
The Relationship

Successful navigation requires a constantly updated neural representation of directional heading, which is conveyed by head direction (HD) cells. The HD signal is predominantly controlled by visual landmarks, but when familiar landmarks are unavailable, self-motion cues are able to control the HD signal via path integration. Previous studies of the relationship between HD cell activity and path integration have been limited to two or more arenas located in the same room, a drawback for interpretation because the same visual cues may have been perceptible across arenas. To address this issue, we tested the relationship between HD cell activity and path integration by recording HD cells while rats navigated within a 14-unit T-maze and in a multiroom maze that consisted of unique arenas that were located in different rooms but connected by a passageway. In the 14-unit T-maze, the HD signal remained relatively stable between the start and goal boxes, with the preferred firing directions usually shifting <45° during maze traversal. In the multiroom maze in light, the preferred firing directions also remained relatively constant between rooms, but with greater variability than in the 14-unit maze. In darkness, HD cell preferred firing directions showed marginally more variability between rooms than in the lighted condition. Overall, the results indicate that self-motion cues are capable of maintaining the HD cell signal in the absence of familiar visual cues, although there are limits to its accuracy. In addition, visual information, even when unfamiliar, can increase the precision of directional perception.

scholarly journals Spike interval coding of translatory optic flow and depth from motion in the fly visual system

2016 ◽  
Author(s):  
Kit D. Longden ◽  
Martina Wicklein ◽  
Benjamin J. Hardcastle ◽  
Stephen J. Huston ◽  
Holger G. Krapp
Keyword(s):  
Optic Flow ◽  
Visual Processing ◽  
Visual Motion ◽  
Receptive Fields ◽  
Cell Types ◽  
Spike Burst ◽  
Cluttered Environments ◽  
Single Spike ◽  
Self Motion ◽  
Spike Bursts

SummaryMany animals use the visual motion generated by travelling in a line, the translatory optic flow, to successfully navigate obstacles: near objects appear larger and to move more quickly than distant ones. Flies are experts at navigating cluttered environments, and while their visual processing of rotatory optic flow is understood in exquisite detail, how they process translatory optic flow remains a mystery. Here, we present novel cell types that have motion receptive fields matched to translation self-motion, the vertical translation (VT) cells. One of these, the VT1 cell, encodes forwards sideslip self-motion, and fires action potentials in clusters of spikes, spike bursts. We show that the spike burst coding is size and speed-tuned, and is selectively modulated by parallax motion, the relative motion experienced during translation. These properties are spatially organized, so that the cell is most excited by clutter rather than isolated objects. When the fly is presented with a simulation of flying past an elevated object, the spike burst activity is modulated by the height of the object, and the single spike rate is unaffected. When the moving object alone is experienced, the cell is weakly driven. Meanwhile, the VT2-3 cells have motion receptive fields matched to the lift axis. In conjunction with previously described horizontal cells, the VT cells have the properties required for the fly to successfully navigate clutter and encode its movements along near cardinal axes of thrust, lift and forward sideslip.

scholarly journals The Role of Idiothetic Signals, Landmarks, and Conjunctive Representations in the Development of Place and Head-Direction Cells: A Self-Organizing Neural Network Model

2021 ◽  
Author(s):  
Toby St. Clere Smithe ◽  
Simon M Stringer
Keyword(s):  
Network Model ◽  
Signal Propagation ◽  
Cell Types ◽  
Visual Signals ◽  
Mammalian Brain ◽  
Head Direction ◽  
State Action ◽  
Attractor Networks ◽  
Planar Velocity ◽  
Self Organizing

Abstract Place and head-direction (HD) cells are fundamental to maintaining accurate representations of location and heading in the mammalian brain across sensory conditions, and are thought to underlie path integration—the ability to maintain an accurate representation of location and heading during motion in the dark. Substantial evidence suggests that both populations of spatial cells function as attractor networks, but their developmental mechanisms are poorly understood. We present simulations of a fully self-organizing attractor network model of this process using well-established neural mechanisms. We show that the differential development of the two cell types can be explained by their different idiothetic inputs, even given identical visual signals: HD cells develop when the population receives angular head velocity input, whereas place cells develop when the idiothetic input encodes planar velocity. Our model explains the functional importance of conjunctive “state-action” cells, implying that signal propagation delays and a competitive learning mechanism are crucial for successful development. Consequently, we explain how insufficiently rich environments result in pathology: place cell development requires proximal landmarks; conversely, HD cells require distal landmarks. Finally, our results suggest that both networks are instantiations of general mechanisms, and we describe their implications for the neurobiology of spatial processing.

scholarly journals The brain compass: a perspective on how self-motion updates the head direction cell attractor

2017 ◽  
Author(s):  
Jean Laurens ◽  
Dora E. Angelaki
Keyword(s):  
Degrees Of Freedom ◽  
Three Dimensional ◽  
Head Tilt ◽  
Head Direction ◽  
Motion Velocity ◽  
Head Direction Cells ◽  
Motion Cues ◽  
Head Direction Cell ◽  
On Line ◽  
Self Motion

ABSTRACTHead Direction cells form an internal compass that signals head azimuth orientation even in the absence of visual landmarks. It is well accepted that head direction properties are generated through a ring attractor that is updated using rotation self-motion cues. The properties and origin of this self-motion velocity drive remain, however, unknown. We propose a unified, quantitative framework whereby the attractor velocity input represents a multisensory self-motion estimate computed through an internal model that uses sensory prediction error based on vestibular, visual, and somatosensory cues to improve on-line motor drive. We show how context-dependent strength of recurrent connections within the attractor itself, rather than the self-motion input, explain differences in head direction cell firing between free foraging and restrained movements. We also summarize recent findings on how head tilt relative to gravity influences the azimuth coding of head direction cells, and explain why and how these effects reflect an updating self-motion velocity drive that is not purely egocentric. Finally, we highlight recent findings that the internal compass may be three-dimensional and hypothesize that the additional vertical degrees of freedom are defined based on global allocentric gravity cues.

scholarly journals Sharp tuning of head direction by somatosensory fast-spiking interneurons

2020 ◽  
Author(s):  
Xiaoyang Long ◽  
Calvin K. Young ◽  
Sheng-Jia Zhang
Keyword(s):  
Cell Types ◽  
Inhibitory Neurons ◽  
Local Network ◽  
Head Direction ◽  
Layer 4 ◽  
Fast Spiking ◽  
External Stimuli ◽  
The Brain ◽  
Spatial Cell

AbstractHead direction (HD) information is intricately linked to spatial navigation and cognition. We recently reported the co-existence of all currently recognized spatial cell types can be found in the hindlimb primary somatosensory cortex (S1HL). In this study, we carried out an in-depth characterization of HD cells in S1HL. We show fast-spiking (FS), putative inhibitory neurons are over-represented in and sharply tuned to HD compared to regular-spiking (RS), putative excitatory neurons. These FS HD cells are non-conjunctive, rarely theta modulated, not locally connected and are enriched in layer 4/5a. Their co-existence with RS HD cells and angular head velocity (AHV) cells in a layer-specific fashion through the S1HL presents a previously unreported organization of spatial circuits. These findings challenge the notion that FS, putative inhibitory interneurons are weakly tuned to external stimuli in general and present a novel local network configuration not reported in other parts of the brain.

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