scholarly journals Passive Movements of the Head Do Not Abolish Anticipatory Firing Properties of Head Direction Cells

2005 ◽  
Vol 93 (3) ◽  
pp. 1304-1316 ◽  
Author(s):  
Joshua P. Bassett ◽  
Michaël B. Zugaro ◽  
Gary M. Muir ◽  
Edward J. Golob ◽  
Robert U. Muller ◽  
...  
Keyword(s):  
Thalamic Nucleus ◽  
Passive Movement ◽  
Efference Copy ◽  
Time Interval ◽  
Head Direction ◽  
Preferred Direction ◽  
Cell Firing ◽  
Firing Properties ◽  
Passive Movements ◽  
Active Contribution

Neurons in the anterior dorsal thalamic nucleus (ADN) of the rat selectively discharge in relation to the animal's head direction (HD) in the horizontal plane. Temporal analyses of cell firing properties reveal that their discharge is optimally correlated with the animal's future directional heading by ∼24 ms. Among the hypotheses proposed to explain this property is that ADN HD cells are informed of future head movement via motor efference copy signals. One prediction of this hypothesis is that when the rat's head is moved passively, the anticipatory time interval (ATI) will be attenuated because the motor efference signal reflects only the active contribution to the movement. The present study tested this hypothesis by loosely restraining the animal and passively rotating it through the cell's preferred direction. Contrary to our prediction, we found that ATI values did not decrease during passive movement but in fact increased significantly. HD cells in the postsubiculum did not show the same effect, suggesting independence between the two sites with respect to anticipatory firing. We conclude that it is unlikely that a motor efference copy signal alone is responsible for generating anticipatory firing in ADN HD cells.

scholarly journals Interspike Interval Analyses Reveal Irregular Firing Patterns at Short, But Not Long, Intervals in Rat Head Direction Cells

2010 ◽  
Vol 104 (3) ◽  
pp. 1635-1648 ◽  
Author(s):  
Jeffrey S. Taube
Keyword(s):  
Interspike Interval ◽  
Grid Cell ◽  
Constant Stimulus ◽  
Head Direction ◽  
Cortical Cells ◽  
Preferred Direction ◽  
Wide Range ◽  
Cell Firing ◽  
Firing Properties ◽  
Irregular Firing

Previous studies have shown that a subset of neurons in the rat anterodorsal thalamus discharge as a function of the animal's head direction (HD) in the horizontal plane, independent of the animal's location and behavior. These cells have consistent firing properties across a wide range of conditions and cell discharge appears highly regular when listened to through a loudspeaker. In contrast, interspike interval (ISI) analyses on cortical cells have found that cell firing is irregular, even under constant stimulus conditions. Here, we analyzed HD cells from the anterodorsal thalamus, while rats foraged for food pellets, to determine whether their firing was regular or irregular. ISIs were measured when the animal's HD was maintained within ±6° of the cell's preferred firing direction. ISIs were highly variable with a mean coefficient of variation (CV) of 0.681. For each cell, the CV values at HDs ±24° away from the cell's preferred direction were similar to the coefficient measured at the cell's preferred direction. A second recording session showed that cells had similar coefficients of variation as the first session, suggesting that the degree of variability in cell spiking was a characteristic property for each cell. There was little correlation between ISIs and angular head velocity or translational speed. ISIs measured in HD cells from the postsubiculum and lateral mammillary nuclei showed higher CV values. These results indicate that despite the appearance of regularity in their firing, HD cells, like cortical cells, have irregular ISIs. In contrast to the irregular firing observed for ISIs, analyses over longer time intervals indicated that HD cell firing was much more regular, more nearly resembling a rate code. These findings have implications for attractor networks that model the HD signal and for models proposed to explain the generation of grid cell signals in entorhinal cortex.

scholarly journals Responses of somatosensory area 2 neurons to actively and passively generated limb movements

2013 ◽  
Vol 109 (6) ◽  
pp. 1505-1513 ◽  
Author(s):  
Brian M. London ◽  
Lee E. Miller
Keyword(s):  
Motor Command ◽  
Accurate Estimate ◽  
Passive Movement ◽  
Efference Copy ◽  
Forward Model ◽  
Sensor Data ◽  
Active Movement ◽  
Noisy Input ◽  
Neural Discharge ◽  
Passive Movements

Control of reaching movements requires an accurate estimate of the state of the limb, yet sensory signals are inherently noisy, because of both noise at the receptors themselves and the stochastic nature of the information representation by neural discharge. One way to derive an accurate representation from noisy sensor data is to combine it with the output of a forward model that considers both the previous state estimate and the noisy input. We recorded from primary somatosensory cortex (S1) in macaques ( Macaca mulatta) during both active and passive movements to investigate how the proprioceptive representation of movement in S1 may be modified by the motor command (through efference copy). We found neurons in S1 that respond to one or both movement types covering a broad distribution from active movement only, to both, to passive movement only. Those neurons that responded to both active and passive movements responded with similar directional tuning. Confirming earlier results, some, but not all, neurons responded before the onset of volitional movements, possibly as a result of efference copy. Consequently, many of the features necessary to combine the forward model with proprioceptive feedback appear to be present in S1. These features would not be expected from combinations of afferent receptor responses alone.

scholarly journals Active and passive movement are encoded equally by head direction cells in the anterodorsal thalamus

2011 ◽  
Vol 106 (2) ◽  
pp. 788-800 ◽  
Author(s):  
Michael E. Shinder ◽  
Jeffrey S. Taube
Keyword(s):  
Body Movement ◽  
Significant Inhibition ◽  
Passive Movement ◽  
Head Direction ◽  
Cell Responses ◽  
Preferred Direction ◽  
Passive Restraint ◽  
System Input ◽  
Proprioceptive Inputs ◽  
Necessary And Sufficient

The head direction (HD) system is composed of cells that represent the direction in which the animal's head is facing. Each HD cell responds optimally when the head is pointing in a particular, or preferred, direction. Although vestibular system input is necessary to generate the directional signal, motor/proprioceptive inputs can also influence HD cell responses. Previous studies comparing active and passive movement have reported significant suppression of the HD signal during passive restraint. However, in each of these studies there was considerable variability across cells, and the animal's head was never completely fixed. To address these issues, we developed a passive restraint system that more fully prevented head and body movement. HD cell responses in the anterodorsal thalamus (ADN) were evaluated during active and passive movement with this new system. Contrary to previous reports, HD cell responses were not affected by passive restraint. Both head-fixed and hand-held restraint failed to produce significant inhibition of the active HD cell response. Furthermore, direction-specific firing was maintained regardless of 1) the animal's previous experience with restraint, 2) whether it was tested in the light or dark, or 3) the position of the animal relative to the axis of rotation. The maintenance of a stable directional signal without appropriate motor, proprioceptive, or visual input indicates that vestibular input is necessary and sufficient for the generation of the HD signal. Motor and proprioceptive influences may therefore be important for the control of the preferred firing direction of HD cells, but not the generation of the signal itself.

Anticipation in the Rodent Head Direction System Can Be Explained by an Interaction of Head Movements and Vestibular Firing Properties

2007 ◽  
Vol 98 (4) ◽  
pp. 1883-1897 ◽  
Author(s):  
Matthijs A. A. van der Meer ◽  
James J. Knierim ◽  
D. Yoganarasimha ◽  
Emma R. Wood ◽  
Mark C. W. van Rossum
Keyword(s):  
Vestibular Nucleus ◽  
Passive Movement ◽  
Head Movements ◽  
Medial Vestibular Nucleus ◽  
Electrophysiological Recording ◽  
Head Direction ◽  
Movement Data ◽  
Behavioral Variables ◽  
Firing Properties ◽  
Functional Circuitry

The rodent head-direction (HD) system, which codes for the animal's head direction in the horizontal plane, is thought to be critically involved in spatial navigation. Electrophysiological recording studies have shown that HD cells can anticipate the animal's HD by up to 75–80 ms. The origin of this anticipation is poorly understood. In this modeling study, we provide a novel explanation for HD anticipation that relies on the firing properties of neurons afferent to the HD system. By incorporating spike rate adaptation and postinhibitory rebound as observed in medial vestibular nucleus neurons, our model produces realistic anticipation on a large corpus of rat movement data. In addition, HD anticipation varies between recording sessions of the same cell, between active and passive movement, and between different studies. Such differences do not appear to be correlated with behavioral variables and cannot be accounted for using earlier models. In the present model, anticipation depends on the power spectrum of the head movements. By direct comparison with recording data, we show that the model explains 60–80% of the observed anticipation variability. We conclude that HD afferent dynamics and the statistics of rat head movements are important in generating HD anticipation. This result contributes to understanding the functional circuitry of the HD system and has methodological implications for studies of HD anticipation.

scholarly journals Passive Transport Disrupts Directional Path Integration by Rat Head Direction Cells

2003 ◽  
Vol 90 (5) ◽  
pp. 2862-2874 ◽  
Author(s):  
Robert W. Stackman ◽  
Edward J. Golob ◽  
Joshua P. Bassett ◽  
Jeffrey S. Taube
Keyword(s):  
Optic Flow ◽  
Path Integration ◽  
Efference Copy ◽  
The Novel ◽  
Head Direction ◽  
Passive Transport ◽  
Novel Environment ◽  
Preferred Direction ◽  
Idiothetic Cues ◽  
Familiar Environment

A subset of neurons in the rat limbic system encodes head direction (HD) by selectively discharging when the rat points its head in a preferred direction in the horizontal plane. The preferred firing direction is sensitive to the location of landmark cues, as well as idiothetic or self-motion cues (i.e., vestibular, motor efference copy, proprioception, and optic flow). Previous studies have shown that the preferred firing direction remains relatively stable (average shift ± 18°) after the rat walks from a familiar environment into a novel one, suggesting that without familiar landmarks, the preferred firing direction can be maintained using idiothetic cues, a process called directional path integration. This study repeated this experiment and manipulated the idiothetic cues available to the rat as it moved between the familiar and novel environment. Motor efference copy/proprioceptive cues were disrupted by passively transporting the animal between the familiar and novel environment. Darkening the room as the animal moved to the novel environment eliminated optic flow cues. HD cell preferred firing directions shifted in the novel environment by an average of 30° after locomotion from the familiar environment with the room lights off; by an average of 70° after passive transport from the familiar environment with the room lights on; and by an average of 67° after passive transport with the room lights off. These findings are consistent with the view that motor efference copy/proprioception cues are important for maintaining the preferred firing direction of HD cells under conditions requiring path integration.

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 Modeling Attractor Deformation in the Rodent Head-Direction System

2000 ◽  
Vol 83 (6) ◽  
pp. 3402-3410 ◽  
Author(s):  
Jeremy P. Goodridge ◽  
David S. Touretzky
Keyword(s):  
Angular Velocity ◽  
Primary Source ◽  
Inhibitory Neurons ◽  
Surprising Result ◽  
Head Direction ◽  
Anterior Thalamus ◽  
Attractor Dynamics ◽  
Cell Firing

We present a model of the head-direction circuit in the rat that improves on earlier models in several respects. First, it provides an account of some of the unique characteristics of head-direction (HD) cell firing in the lateral mammillary nucleus and the anterior thalamus. Second, the model functions without making physiologically unrealistic assumptions. In particular, it implements attractor dynamics in postsubiculum and lateral mammillary nucleus without directionally tuned inhibitory neurons, which have never been observed in vivo, and it integrates angular velocity without the use of multiplicative synapses. The model allows us to examine the relationships among three HD areas and various properties of their representations. A surprising result is that certain combinations of purported HD cell properties are mutually incompatible, suggesting that the lateral mammillary nucleus may not be the primary source of head direction input to anterior thalamic HD cells.

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