The Nucleus Prepositus Hypoglossi Contributes to Head Direction Cell Stability in Rats (original) (raw)

Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input

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 supragenual nucleus: A putative relay station for ascending vestibular signs to head direction cells

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.

Head direction cell activity in the anterodorsal thalamus requires intact supragenual nuclei

Journal of Neurophysiology, 2012

Neural activity in several limbic areas varies as a function of the animal's head direction (HD) in the horizontal plane. Lesions of the vestibular periphery abolish this HD cell signal, suggesting an essential role for vestibular afference in HD signal generation. The organization of brain stem pathways conveying vestibular information to the HD circuit is poorly understood; however, recent anatomical work has identified the supragenual nucleus (SGN) as a putative relay. To test this hypothesis, we made lesions of the SGN in rats and screened for HD cells in the anterodorsal thalamus. In animals with complete bilateral lesions, the overall number of HD cells was significantly reduced relative to control animals. In animals with unilateral lesions of the SGN, directional activity was present, but the preferred firing directions of these cells were unstable and less influenced by the rotation of an environmental landmark. In addition, we found that preferred directions displayed large directional shifts when animals foraged for food in a darkened environment and when they were navigating from a familiar environment to a novel one, suggesting that the SGN plays a critical role in projecting essential self-motion (idiothetic) information to the HD cell circuit.

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...

Does the vestibular system contribute to head direction cell activity in the rat?

Physiology & Behavior, 2002

Head direction cells (HDC) located in several regions of the brain, including the anterior dorsal nucleus of the thalamus (ADN), postsubiculum (PoS), and lateral mammillary nuclei (LMN), provide the neural substrate for the determination of head direction. Although activity of HDC is influenced by various sensory signals and internally generated cues, lesion studies and some anatomical and physiological evidence suggest that vestibular inputs are critical for the maintenance of directional sensitivity of these cells. However, vestibular inputs must be transformed considerably in order to signal head direction, and the neuronal circuitry that accomplishes this signal processing has not been fully established. Furthermore, it is unclear why the removal of vestibular inputs abolishes the directional sensitivity of HDC, as visual and other sensory inputs and motor feedback signals strongly affect the firing of these neurons and would be expected to maintain their directional-related activity. Further physiological studies will be required to establish the role of vestibular system in producing HDC responses, and anatomical studies are needed to determine the neural circuitry that mediates vestibular influences on determination of head direction. D

Head Direction Cell Instability in the Anterior Dorsal Thalamus after Lesions of the Interpeduncular Nucleus

Journal of Neuroscience, 2009

Previous research has identified a population of cells throughout the limbic system that discharge as a function of the animal's head direction (HD). Altering normal motor cues can alter the HD cell responses and disrupt the updating of their preferred firing directions, thus suggesting that motor cues contribute to processing the HD signal. A pathway that conveys motor information may stem from the interpeduncular nucleus (IPN), a brain region that has reciprocal connections with HD cell circuitry. To test this hypothesis, we produced electrolytic or neurotoxic lesions of the IPN and recorded HD cells in the anterior dorsal thalamus (ADN) of rats. Direction-specific firing remained present in the ADN after lesions of the IPN, but measures of HD cell properties showed that cells had reduced peak firing rates, large directional firing ranges, and firing that predicted the animal's future heading more than in intact controls. Furthermore, preferred firing directions were moderately less influenced by rotation of a salient visual landmark. Finally, the preferred directions of cells in lesioned rats exhibited large shifts when the animals foraged for scattered food pellets in a darkened environment and when locomoting from a familiar environment to a novel one. We propose that the IPN contributes motor information about the animal's movements to the HD cell circuitry. Furthermore, these results suggest that the IPN plays a broad role in the discharge properties and stability of directionspecific activity in the HD cell circuit.

Recordings of postsubiculum head direction cells following lesions of the laterodorsal thalamic nucleus

Brain Research, 1998

Areas of the rodent limbic system are important for solving spatial tasks and accurate navigation. Previous studies have identified cells Ž . Ž . in the postsubiculum PoS and the lateral dorsal thalamus LDN which discharge as a function of the animal's head direction in the horizontal plane. These two brain areas are reciprocally connected with one another. To determine the contribution of the LDN to the functioning of PoS head direction cells, we lesioned the LDN and recorded single units in the PoS. We report here that lesions of the LDN had little effect upon the firing properties of PoS HD cells. In addition, HD cells from lesioned animals showed normal responses to Ž . two environmental manipulations: 1 when the salient visual cue was rotated the preferred firing directions of PoS HD cells shifted a Ž . similar amount and 2 cells frequently ceased firing, or had reductions in their peak firing rate, when the animal was restrained and passively rotated through the preferred firing direction. These results indicate that the LDN does not play a substantive role in either the generation or the stability of the HD cell signal in the PoS. q 1998 Elsevier Science B.V.

Directional preference of otolith-related neurons in vestibular nucleus

2020

Background: Due to the paired structure of two labyrinths at both sides of ear, their communication is conducted through the interconnected commissural pathway. The close interconnection produces the neural responding property in vestibular nucleus, and the mechanical movement of the hair cells mainly specifies the property. However, the mechanism to initiate the responding property was evident based on the structure, but few direct experimental data were provided to understand the responding property based on the structure. Experimental Approach: The directional preference was investigated, which was one of critical neural responding property to illustrate the functional structure. Also, a chemically induced unilateral labyrinthectomy (UL) was performed to emphasize the preference. For the model evaluation, static and dynamic behavioral tests were applied, and the results demonstrated a practical model construction. Following the evaluation, an extracellular neural activity was conducted for the neuronal responses to the horizontal head rotation and the linear head movement. Results: Seventy seven neuronal activities were recorded from thirty SD rats (270-450 g, male), and total population was divided into three groups; left UL (20), sham (35), right UL (22). Based on the directional preference, two subgroups were again classified as contra-and ipsi-preferred neurons. There was no significance between those subgroups (contra-: 15/35, 43%; ipsi-: 20/35, 57%) in sham model. However, more ipsi-preferred neurons (19/22, 86%) were observed after right UL while left UL caused more contra-preferred neurons (13/20, 65%). In particular, the convergent neurons mainly led this biased difference in the population (ipsi-: 100% after right UL & contra-: 89% after left UL). Conclusion: The directional preference was evenly maintained under a normal vestibular function, and its unilateral loss biased the directional preference of the neurons, depending on the side of lesion. Moreover, the dominance of the directional preference was mainly led by the convergent neurons which had the neural information related with head rotation and linear translation. Background Vestibular nucleus (VN) is the core neural complex which the initial neural signals from different body structures are processed and converged. As two labyrinths are separately positioned at both sides of

Medial vestibular nucleus in the guinea-pig

Experimental Brain Research, 1991

Intracellular recordings were obtained from medial vestibular nuclei neurones (MVNn) in guinea-pig brainstem slices. Two main distinct neuronal classes were encountered. Type A MVNn (32.3 %) were characterized by a broad action potential followed by a deep single afterhyperpolarization, a transient A-like rectification, and a single range of firing in response to current injection. Type B MVNn (47.1%), in contrast, were distinguished by the presence of a thin action potential followed first by a fast and then by a delayed and slower afterhyperpolarization. In addition, they displayed a secondary range of firing in their response to current injection. A majority of B MVNn also had either subthreshold plateau potentials or low threshold spike bursts or a combination thereof. A third, non-homogeneous class of cells, could not be fitted into either one of the two main classes (20.6%, type C MVNn).