Does the vestibular system contribute to head direction cell activity in the rat? (original) (raw)
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The Journal of neuroscience : the official journal of the Society for Neuroscience, 1997
Vestibular information influences spatial orientation and navigation in laboratory animals and humans. Neurons within the rat anterior thalamus encode the directional heading of the animal in absolute space. These neurons, referred to as head direction (HD) cells, fire selectively when the rat points its head in a specific direction in the horizontal plane with respect to the external laboratory reference frame. HD cells are thought to represent an essential component of a neural network that processes allocentric spatial information. The functional properties of HD cells may be dependent on vestibular input. Here, anterior thalamic HD cells were recorded before and after sodium arsanilate-induced vestibular system lesion. Vestibular lesions abolished the directional firing properties of HD cells. The time course of disruption in the directional firing properties paralleled the loss of vestibular function. Arsanilate-treated rats exhibited only minor changes in locomotor behavior, w...
The vestibular contribution to the head direction signal and navigation
Frontiers in Integrative Neuroscience, 2014
Spatial learning and navigation depend on neural representations of location and direction within the environment. These representations, encoded by place cells and head direction (HD) cells, respectively, are dominantly controlled by visual cues, but require input from the vestibular system. Vestibular signals play an important role in forming spatial representations in both visual and non-visual environments, but the details of this vestibular contribution are not fully understood. Here, we review the role of the vestibular system in generating various spatial signals in rodents, focusing primarily on HD cells. We also examine the vestibular system's role in navigation and the possible pathways by which vestibular information is conveyed to higher navigation centers.
Brain Research, 2006
Head direction (HD) cells located in several regions of the brain, including the postsubiculum, retrosplenial cortex, lateral dorsal thalamic nucleus, anterior dorsal thalamic nucleus, and lateral mammillary nucleus, provide a signal of the rat's momentary directional heading. Experimental evidence suggests that vestibular inputs are critical for the maintenance these cells' directional sensitivity. However, it is still unclear how vestibular information is conveyed to the HD cell-related circuitry. In a recent study, the supragenual nucleus (SG) was suggested as a putative relay of vestibular inputs to this circuitry. In the present study, using anterograde and retrograde tract-tracing methods, we first investigated whether the SG is in a position to convey vestibular inputs. Next, we examined the projections of the SG with the Phaseolus vulgaris leucoagglutinin method. Our results indicate that the SG receives direct inputs from the medial vestibular nucleus and projects to elements of the HD cell-related circuitry, providing a massive input to the contralateral dorsal tegmental nucleus and a moderately dense projection to the shell region of the lateral mammillary nucleus. Overall, the present findings serve to clarify how vestibular inputs reach the HD cell-related circuit and point out the SG as an important interface to this end.
Effects of body to head rotation on the labyrinthine responses of rat vestibular neurons
Neuroscience, 2013
Vestibulospinal reflexes elicited by head displacement in space depend on the direction of body displacement, because the neuronal responses to labyrinthine stimulation are tuned by neck displacement: a directional tuning takes place in the medial cerebellum and in spinal motoneurons, while a gain and a basal activity tuning can be observed in the reticular formation, a target structure of the medial cerebellum. In the present study, we investigated whether also the response of vestibular nuclear neurons (another target of the medial cerebellum) to labyrinthine stimulation is tuned by neck displacement and which parameters of the response are modulated by it. In urethane-anaesthetized Wistar rats, single-unit activity was recorded from the vestibular nuclei at rest and during wobble of the whole animal at 0.156 Hz. This stimulus tilted the animal's head by a constant amplitude (5°), in a direction rotating at a constant velocity over the horizontal plane, either in clockwise or counter clockwise direction. The gain and the direction of neuronal responses to wobble were evaluated through Fourier analysis, in the control position (with coincident head and body axes) and following a body-to-head rotation of 5-30°over the horizontal plane, in both directions. Most of the vestibular neurons modified their response gain and/or their basal activity following body-to-head rotation, as it occurs in the reticular formation. Only few neurons modified their response direction, as occurs in the cerebellum and in spinal motoneurons. The different behaviour of cerebellar neurons and of their vestibular and reticular target cells, suggests that the role played by the cerebellum in the neck tuning of vestibulospinal reflexes has to be reconsidered. Ó
Head Direction Cell Activity in Mice: Robust Directional Signal Depends on Intact Otolith Organs
Journal of Neuroscience - J NEUROSCI, 2009
The head direction (HD) cell signal is a representation of an animal's perceived directional heading with respect to its environment. This signal appears to originate in the vestibular system, which includes the semicircular canals and otolith organs. Preliminary studies indicate the semicircular canals provide a necessary component of the HD signal, but involvement of otolithic information in the HD signal has not been tested. The present study was designed to determine the otolithic contribution to the HD signal, as well as to compare HD cell activity of mice to that of rats. HD cell activity in the anterodorsal thalamus was assessed in wild-type C57BL/6J and otoconia-deficient tilted mice during locomotion within a cylinder containing a prominent visual landmark. HD cell firing properties in C57BL/6J mice were generally similar to those in rats. However, in C57BL/6J mice, landmark rotation failed to demonstrate dominant control of the HD signal in 36% of the sessions. In darkness, directional firing became unstable during 42% of the sessions, but landmark control was not associated with HD signal stability in darkness. HD cells were identified in tilted mice, but directional firing properties were not as robust as those of C57BL/6J mice. Most HD cells in tilted mice were controlled by landmark rotation, but showed substantial signal degradation across trials. These results support current models that suggest otolithic information is involved in the perception of directional heading. Furthermore, compared to rats, the HD signal in mice appears to be less reliably anchored to prominent environmental cues.
Direction Discrimination Thresholds of Vestibular and Cerebellar Nuclei Neurons
Journal of Neuroscience, 2010
McCrea, Robert A., Greg T. Gdowski, Richard Boyle, and Timothy Belton. Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons. J. Neurophysiol. 82: 416-428, 1999. The firing behavior of 51 non-eye movement related central vestibular neurons that were sensitive to passive head rotation in the plane of the horizontal semicircular canal was studied in three squirrel monkeys whose heads were free to move in the horizontal plane. Unit sensitivity to active head movements during spontaneous gaze saccades was compared with sensitivity to passive head rotation. Most units (29/35 tested) were activated at monosynaptic latencies following electrical stimulation of the ipsilateral vestibular nerve. Nine were vestibulo-spinal units that were antidromically activated following electrical stimulation of the ventromedial funiculi of the spinal cord at C1. All of the units were less sensitive to active head movements than to passive whole body rotation. In the majority of cells (37/51, 73%), including all nine identified vestibulo-spinal units, the vestibular signals related to active head movements were canceled. The remaining units (n ϭ 14, 27%) were sensitive to active head movements, but their responses were attenuated by 20-75%. Most units were nearly as sensitive to passive head-on-trunk rotation as they were to whole body rotation; this suggests that vestibular signals related to active head movements were cancelled primarily by subtraction of a head movement efference copy signal. The sensitivity of most units to passive whole body rotation was unchanged during gaze saccades. A fundamental feature of sensory processing is the ability to distinguish between self-generated and externally induced sensory events. Our observations suggest that the distinction is made at an early stage of processing in the vestibular system.
Angular head velocity cells within brainstem nuclei projecting to the head direction circuit
An animal’s perceived sense of orientation depends upon the head direction (HD) system found in several limbic structures and depends upon an intact peripheral vestibular labyrinth. However, how the vestibular system influences the generation, maintenance, and updating of the HD signal remains poorly understood. Anatomical and lesion studies point towards three key brainstem nuclei as being potential critical components in generating the HD signal: nucleus prepositus hypoglossi (NPH), supragenual nucleus (SGN), and dorsal paragigantocellularis reticular nuclei (PGRNd). Collectively, these nuclei are situated between the vestibular nuclei and the dorsal tegmental and lateral mammillary nuclei, which are thought to serve as the origin of the HD signal. To test this hypothesis, extracellular recordings were made in these areas while rats either freely foraged in a cylindrical environment or were restrained and rotated passively. During foraging, a large subset of cells in all three nuc...
Vestibular and attractor network basis of the head direction cell signal in subcortical circuits
Frontiers in Neural Circuits, 2012
Accurate navigation depends on a network of neural systems that encode the moment-to-moment changes in an animal's directional orientation and location in space. Within this navigation system are head direction (HD) cells, which fire persistently when an animal's head is pointed in a particular direction . HD cells are widely thought to underlie an animal's sense of spatial orientation, and research over the last 25+ years has revealed that this robust spatial signal is widely distributed across subcortical and cortical limbic areas. The purpose of the present review is to summarize some of the recent studies arguing that the origin of the HD signal resides subcortically, specifically within the reciprocal connections of the dorsal tegmental and lateral mammillary nuclei. Furthermore, we review recent work identifying "bursting" cellular activity in the HD cell circuit after lesions of the vestibular system, and relate these observations to the long held view that attractor network mechanisms underlie HD signal generation. Finally, we summarize anatomical and physiological work suggesting that this attractor network architecture may reside within the tegmento-mammillary circuit.
The Nucleus Prepositus Hypoglossi Contributes to Head Direction Cell Stability in Rats
The Journal of Neuroscience, 2015
Head direction (HD) cells in the rat limbic system fire according to the animal's orientation independently of the animal's environmental location or behavior. These HD cells receive strong inputs from the vestibular system, among other areas, as evidenced by disruption of their directional firing after lesions or inactivation of vestibular inputs. Two brainstem nuclei, the supragenual nucleus (SGN) and nucleus prepositus hypoglossi (NPH), are known to project to the HD network and are thought to be possible relays of vestibular information. Previous work has shown that lesioning the SGN leads to a loss of spatial tuning in downstream HD cells, but the NPH has historically been defined as an oculomotor nuclei and therefore its role in contributing to the HD signal is less clear. Here, we investigated this role by recording HD cells in the anterior thalamus after either neurotoxic or electrolytic lesions of the NPH. There was a total loss of direction-specific firing in anterodorsal thalamus cells in animals with complete NPH lesions. However, many cells were identified that fired in bursts unrelated to the animals' directional heading and were similar to cells seen in previous studies that damaged vestibularassociated areas. Some animals with significant but incomplete lesions of the NPH had HD cells that were stable under normal conditions, but were unstable under conditions designed to minimize the use of external cues. These results support the hypothesis that the NPH, beyond its traditional oculomotor function, plays a critical role in conveying vestibular-related information to the HD circuit.