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1.
J Neurosci ; 44(10)2024 Mar 06.
Artigo em Inglês | MEDLINE | ID: mdl-38286624

RESUMO

Navigating a complex world requires integration of multiple spatial reference frames, including information about one's orientation in both allocentric and egocentric coordinates. Combining these two information sources can provide additional information about one's spatial location. Previous studies have demonstrated that both egocentric and allocentric spatial signals are reflected by the firing of neurons in the rat postrhinal cortex (POR), an area that may serve as a hub for integrating allocentric head direction (HD) cell information with egocentric information from center-bearing and center-distance cells. However, we have also demonstrated that POR HD cells are uniquely influenced by the visual properties and locations of visual landmarks, bringing into question whether the POR HD signal is truly allocentric as opposed to simply being a response to visual stimuli. To investigate this issue, we recorded HD cells from the POR of female rats while bilaterally inactivating the anterior thalamus (ATN), a region critical for expression of the "classic" HD signal in cortical areas. We found that ATN inactivation led to a significant decrease in both firing rate and tuning strength for POR HD cells, as well as a disruption in the encoding of allocentric location by conjunctive HD/egocentric cells. In contrast, POR egocentric cells without HD tuning were largely unaffected in a consistent manner by ATN inactivation. These results indicate that the POR HD signal originates at least partially from projections from the ATN and supports the view that the POR acts as a hub for the integration of egocentric and allocentric spatial representations.


Assuntos
Núcleos Anteriores do Tálamo , Ratos , Feminino , Animais , Orientação/fisiologia , Percepção Espacial/fisiologia
2.
J Neurosci ; 43(49): 8403-8424, 2023 12 06.
Artigo em Inglês | MEDLINE | ID: mdl-37871964

RESUMO

The sense of orientation of an animal is derived from the head direction (HD) system found in several limbic structures and depends on an intact vestibular labyrinth. However, how the vestibular system influences the generation and updating of the HD signal remains poorly understood. Anatomical and lesion studies point toward three key brainstem nuclei as key components for generating the HD signal-nucleus prepositus hypoglossi, supragenual nucleus, and dorsal paragigantocellularis reticular nuclei. 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 determine the types of information these brain areas convey to the HD network, we recorded neurons from these regions while female rats actively foraged in a cylindrical enclosure or were restrained and rotated passively. During foraging, a large subset of cells in all three nuclei exhibited activity that correlated with the angular head velocity (AHV) of the rat. Two fundamental types of AHV cells were observed; (1) symmetrical AHV cells increased or decreased their firing with increases in AHV regardless of the direction of rotation, and (2) asymmetrical AHV cells responded differentially to clockwise and counterclockwise head rotations. When rats were passively rotated, some AHV cells remained sensitive to AHV, whereas firing was attenuated in other cells. In addition, a large number of AHV cells were modulated by linear head velocity. These results indicate the types of information conveyed from the vestibular nuclei that are responsible for generating the HD signal.SIGNIFICANCE STATEMENT Extracellular recording of brainstem nuclei (nucleus prepositus hypoglossi, supragenual nucleus, and dorsal paragigantocellularis reticular nucleus) that project to the head direction circuit identified different types of AHV cells while rats freely foraged in a cylindrical environment. The firing of many cells was also modulated by linear velocity. When rats were restrained and passively rotated, some cells remained sensitive to AHV, whereas others had attenuated firing. These brainstem nuclei provide critical information about the rotational movement of the head of the rat in the azimuthal plane.


Assuntos
Movimento , Neurônios , Ratos , Feminino , Animais , Movimento/fisiologia , Neurônios/fisiologia , Núcleos Vestibulares , Núcleo Celular , Movimentos da Cabeça/fisiologia , Cabeça/fisiologia
3.
Hippocampus ; 34(4): 168-196, 2024 Apr.
Artigo em Inglês | MEDLINE | ID: mdl-38178693

RESUMO

Head direction (HD) cells, which fire persistently when an animal's head is pointed in a particular direction, are widely thought to underlie an animal's sense of spatial orientation and have been identified in several limbic brain regions. Robust HD cell firing is observed throughout the thalamo-parahippocampal system, although recent studies report that parahippocampal HD cells exhibit distinct firing properties, including conjunctive aspects with other spatial parameters, which suggest they play a specialized role in spatial processing. Few studies, however, have quantified these apparent differences. Here, we performed a comparative assessment of HD cell firing characteristics across the anterior dorsal thalamus (ADN), postsubiculum (PoS), parasubiculum (PaS), medial entorhinal (MEC), and postrhinal (POR) cortices. We report that HD cells with a high degree of directional specificity were observed in all five brain regions, but ADN HD cells display greater sharpness and stability in their preferred directions, and greater anticipation of future headings compared to parahippocampal regions. Additional analysis indicated that POR HD cells were more coarsely modulated by other spatial parameters compared to PoS, PaS, and MEC. Finally, our analyses indicated that the sharpness of HD tuning decreased as a function of laminar position and conjunctive coding within the PoS, PaS, and MEC, with cells in the superficial layers along with conjunctive firing properties showing less robust directional tuning. The results are discussed in relation to theories of functional organization of HD cell tuning in thalamo-parahippocampal circuitry.


Assuntos
Núcleos Anteriores do Tálamo , Giro Para-Hipocampal , Animais , Giro Para-Hipocampal/fisiologia , Córtex Cerebral , Percepção Espacial , Cabeça/fisiologia
4.
Hippocampus ; 33(5): 488-504, 2023 05.
Artigo em Inglês | MEDLINE | ID: mdl-36780179

RESUMO

Neurons in the rat postrhinal cortex (POR) respond to the egocentric (observer-centered) bearing and distance of the boundaries, or geometric center, of an enclosed space. Understanding of the precise geometric and sensory properties of the environment that generate these signals is limited. Here we model how this signal may relate to visual perception of motion parallax along environmental boundaries. A behavioral extension of this tuning is the known 'centering response', in which animals follow a spatial gradient function based on boundary parallax to guide behavior toward the center of a corridor or enclosure. Adding an allocentric head direction signal to this representation can translate the gradient across two-dimensional space and provide a new gradient for directing behavior to any location. We propose a model for how this signal may support goal-directed navigation via projections to the dorsomedial striatum. The result is a straightforward code for navigational variables derived from visual geometric properties of the surrounding environment, which may be used to map space and transform incoming sensory information into an appropriate motor output.


Assuntos
Objetivos , Navegação Espacial , Ratos , Animais , Córtex Cerebral/fisiologia , Percepção Visual , Percepção Espacial/fisiologia , Navegação Espacial/fisiologia
5.
Neurobiol Learn Mem ; 189: 107596, 2022 03.
Artigo em Inglês | MEDLINE | ID: mdl-35131453

RESUMO

The postrhinal cortex (POR) serves as a key input area to the hippocampal system. It receives highly processed information from the ventral visual stream and other limbic areas including the retrosplenial cortex, parahippocampal areas, and portions of the limbic thalamus. The POR was studied early on by David Bucci and colleagues who first postulated that the POR plays a major role in contextual learning. Here we review a number of approaches and experimental studies that have explored POR's role in contextual processing. We discuss POR lesion studies that monitored deficits in fear conditioning tasks and the effects that these lesions had on processing visual landmark information. We then review the types of spatial correlates encoded by POR cells. A large number of head direction (HD) cells are present, although recent findings suggest that many of them are more accurately characterized as landmark modulated-HD cells as opposed to classic HD cells. A significant number of POR cells are also tuned to egocentric properties of the environment, such as the spatial relationship of the animal to the center of its environment, or the distance between the animal and either the environment's center or its boundaries. We suggest potential frameworks through which these functional cell types might support contextual processing. We then discuss deficits seen in humans who have damage to the homologous parahippocampal cortex, and we finish by reviewing functional imaging studies that found activation of this area while human subjects performed various tasks. A preponderance of evidence suggests that the POR, along with its interactions with retrosplenial cortex, plays a key role in contextual information processing.


Assuntos
Córtex Cerebral , Medo , Animais , Córtex Cerebral/fisiologia , Cognição , Medo/fisiologia , Hipocampo/fisiologia , Humanos , Aprendizagem/fisiologia
6.
J Neurosci ; 40(15): 3035-3051, 2020 04 08.
Artigo em Inglês | MEDLINE | ID: mdl-32127493

RESUMO

Navigation often requires movement in three-dimensional (3D) space. Recent studies have postulated two different models for how head direction (HD) cells encode 3D space: the rotational plane hypothesis and the dual-axis model. To distinguish these models, we recorded HD cells in female rats while they traveled different routes along both horizontal and vertical surfaces from an elevated platform to the top of a cuboidal apparatus. We compared HD cell preferred firing directions (PFDs) in different planes and addressed the issue of whether HD cell firing is commutative-does the order of the animal's route affect the final outcome of the cell's PFD? Rats locomoted a direct or indirect route from the floor to the cube top via one, two, or three vertical walls. Whereas the rotational plane hypothesis accounted for PFD shifts when the animal traversed horizontal corners, the cell's PFD was better explained by the dual-axis model when the animal traversed vertical corners. Responses also followed the dual-axis model (1) under dark conditions, (2) for passive movement of the rat, (3) following apparatus rotation, (4) for movement around inside vertical corners, and (5) across a 45° outside vertical corner. The order in which the animal traversed the different planes did not affect the outcome of the cell's PFD, indicating that responses were commutative. HD cell peak firing rates were generally equivalent along each surface. These findings indicate that the animal's orientation with respect to gravity plays an important role in determining a cell's PFD, and that vestibular and proprioceptive cues drive these computations.SIGNIFICANCE STATEMENT Navigating in a three-dimensional (3D) world is a complex task that requires one to maintain a proper sense of orientation relative to both local and global cues. Rodent head direction (HD) cells have been suggested to subserve this sense of orientation, but most HD cell studies have focused on navigation in 2D environments. We investigated the responses of HD cells as rats moved between multiple vertically and horizontally oriented planar surfaces, demonstrating that HD cells align their directional representations to both local (current plane of locomotion) and global (gravity) cues across several experimental conditions, including darkness and passive movement. These findings offer critical insights into the processing of 3D space in the mammalian brain.


Assuntos
Movimentos da Cabeça/fisiologia , Locomoção/fisiologia , Percepção Espacial/fisiologia , Animais , Comunicação Celular , Escuridão , Eletrodos Implantados , Fenômenos Eletrofisiológicos , Feminino , Gravitação , Individualidade , Neurônios/fisiologia , Orientação , Propriocepção/fisiologia , Desempenho Psicomotor/fisiologia , Ratos , Ratos Long-Evans , Rotação , Vestíbulo do Labirinto/fisiologia
7.
J Cogn Neurosci ; 33(2): 159-166, 2021 02.
Artigo em Inglês | MEDLINE | ID: mdl-33054553

RESUMO

Real-world navigation requires movement of the body through space, producing a continuous stream of visual and self-motion signals, including proprioceptive, vestibular, and motor efference cues. These multimodal cues are integrated to form a spatial cognitive map, an abstract, amodal representation of the environment. How the brain combines these disparate inputs and the relative importance of these inputs to cognitive map formation and recall are key unresolved questions in cognitive neuroscience. Recent advances in virtual reality technology allow participants to experience body-based cues when virtually navigating, and thus it is now possible to consider these issues in new detail. Here, we discuss a recent publication that addresses some of these issues (D. J. Huffman and A. D. Ekstrom. A modality-independent network underlies the retrieval of large-scale spatial environments in the human brain. Neuron, 104, 611-622, 2019). In doing so, we also review recent progress in the study of human spatial cognition and raise several questions that might be addressed in future studies.


Assuntos
Realidade Virtual , Sinais (Psicologia) , Humanos , Imageamento por Ressonância Magnética , Movimento , Propriocepção
8.
J Neurophysiol ; 123(5): 1808-1827, 2020 05 01.
Artigo em Inglês | MEDLINE | ID: mdl-32208877

RESUMO

A major question in the field of spatial cognition is how animals represent three-dimensional (3D) space. Different results have been obtained across various species and may depend on whether the species inhabits a 3D environment or is terrestrial (land dwelling). The head direction (HD) cell system is an attractive candidate to study in terms of 3D representations. HD cells fire as a function of the animal's directional heading in the horizontal plane, independent of the animal's location and on-going behavior. Another issue concerns whether HD cells are tuned in 3D space or tuned to the 2D horizontal plane. Shinder and Taube (Shinder ME, Taube JS. J Neurophysiol 121: 4-37, 2019) addressed this issue by manipulating a rat's orientation in 3D space while monitoring responses from classic HD cells in the rat anterodorsal thalamus. They reported that HD cells did not display conjunctive firing with pitch or roll orientations. Direction-specific firing was primarily derived from horizontal semicircular canal information and that the gravity vector played an important role in influencing the cell's firing rate and its preferred firing direction. Laurens and Angelaki (Laurens J, Angelaki DE. J Neurophysiol 122: 1274-1287, 2019) challenged this view by performing a mathematical analysis on the Shinder and Taube data and concluded that they would not have seen 3D tuning based on their experimental approach. We provide a historical review of these issues followed by a summary of the experiments, which includes additional analyses. We then define what it means for a HD cell to be tuned in 3D and finish by rebutting the reanalyses performed by Laurens and Angelaki.


Assuntos
Comportamento Animal/fisiologia , Cabeça/fisiologia , Orientação/fisiologia , Células de Lugar/fisiologia , Navegação Espacial/fisiologia , Vestíbulo do Labirinto/fisiologia , Animais , Ratos
9.
J Neurophysiol ; 121(1): 4-37, 2019 01 01.
Artigo em Inglês | MEDLINE | ID: mdl-30379631

RESUMO

Head direction (HD) cells fire when the animal faces that cell's preferred firing direction (PFD) in the horizontal plane. The PFD response when the animal is oriented outside the earth-horizontal plane could result from cells representing direction in the plane of locomotion or as a three-dimensional (3D), global-referenced direction anchored to gravity. To investigate these possibilities, anterodorsal thalamic HD cells were recorded from restrained rats while they were passively positioned in various 3D orientations. Cell responses were unaffected by pitch or roll up to ~90° from the horizontal plane. Firing was disrupted once the animal was oriented >90° away from the horizontal plane and during inversion. When rolling the animal around the earth-vertical axis, cells were active when the animal's ventral surface faced the cell's PFD. However, with the rat rolled 90° in an ear-down orientation, pitching the rat and rotating it around the vertical axis did not produce directionally tuned responses. Complex movements involving combinations of yaw-roll, but usually not yaw-pitch, resulted in reduced directional tuning even at the final upright orientation when the rat had full visual view of its environment and was pointing in the cell's PFD. Directional firing was restored when the rat's head was moved back-and-forth. There was limited evidence indicating that cells contained conjunctive firing with pitch or roll positions. These findings suggest that the brain's representation of directional heading is derived primarily from horizontal canal information and that the HD signal is a 3D gravity-referenced signal anchored to a direction in the horizontal plane. NEW & NOTEWORTHY This study monitored head direction cell responses from rats in three dimensions using a series of manipulations that involved yaw, pitch, roll, or a combination of these rotations. Results showed that head direction responses are consistent with the use of two reference frames simultaneously: one defined by the surrounding environment using primarily visual landmarks and a second defined by the earth's gravity vector.


Assuntos
Percepção de Movimento/fisiologia , Neurônios/fisiologia , Orientação/fisiologia , Percepção Espacial/fisiologia , Tálamo/fisiologia , Potenciais de Ação , Animais , Feminino , Cabeça , Estimulação Física , Propriocepção/fisiologia , Ratos Long-Evans , Restrição Física
10.
J Neurophysiol ; 121(2): 371-395, 2019 02 01.
Artigo em Inglês | MEDLINE | ID: mdl-30427743

RESUMO

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.


Assuntos
Corpo Estriado/fisiologia , Movimentos da Cabeça , Córtex Motor/fisiologia , Neurônios/fisiologia , Animais , Corpo Estriado/citologia , Feminino , Córtex Motor/citologia , Técnicas de Rastreamento Neuroanatômico , Neurônios/citologia , Ratos , Ratos Long-Evans
11.
J Neurophysiol ; 121(2): 350-370, 2019 02 01.
Artigo em Inglês | MEDLINE | ID: mdl-30427767

RESUMO

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.


Assuntos
Corpo Estriado/fisiologia , Movimentos da Cabeça , Córtex Motor/fisiologia , Neurônios/fisiologia , Animais , Corpo Estriado/citologia , Potenciais Evocados , Retroalimentação Fisiológica , Feminino , Córtex Motor/citologia , Ratos , Ratos Long-Evans
12.
J Neurosci ; 36(3): 741-54, 2016 Jan 20.
Artigo em Inglês | MEDLINE | ID: mdl-26791205

RESUMO

Head direction (HD) cells fire when an animal faces a particular direction in its environment, and they are thought to represent the neural correlate of the animal's perceived spatial orientation. Previous studies have shown that vestibular information is critical for generating the HD signal but have not delineated whether information from all three semicircular canals or just the horizontal canals, which are primarily sensitive to angular head rotation in the horizontal (yaw) plane, are critical for the signal. Here, we monitored cell activity in the anterodorsal thalamus (ADN), an area known to contain HD cells, in epstatic circler (Ecl) mice, which have a bilateral malformation of the horizontal (lateral) semicircular canals. Ecl mice and their littermates that did not express the mutation (controls) were implanted with recording electrodes in the ADN. Results confirm the important role the horizontal canals play in forming the HD signal. Although normal HD cell activity (Raleigh's r > 0.4) was recorded in control mice, no such activity was found in Ecl mice, although some cells had activity that was mildly modulated by HD (0.4 > r > 0.2). Importantly, we also observed activity in Ecl mice that was best characterized as bursty--a pattern of activity similar to an HD signal but without any preferred firing direction. These results suggest that the neural structure for the HD network remains intact in Ecl mice, but the absence of normal horizontal canals results in an inability to control the network properly and brings about an unstable HD signal. Significance statement: Cells in the anterior dorsal thalamic nucleus normally fire in relation to the animal's directional heading with respect to the environment--so-called head direction cells. To understand how these head direction cells generate their activity, we recorded single-unit activity from the anterior dorsal thalamus in transgenic mice that lack functional horizontal semicircular canals. We show that the neural network for the head direction signal remains intact in these mice, but that the absence of normal horizontal canals results in an inability to control the network properly and brings about an unstable head direction signal.


Assuntos
Movimentos da Cabeça/fisiologia , Orientação/fisiologia , Canais Semicirculares/patologia , Canais Semicirculares/fisiologia , Animais , Feminino , Hipercinese/patologia , Hipercinese/fisiopatologia , Masculino , Camundongos , Camundongos Endogâmicos C57BL , Camundongos Transgênicos , Canais Semicirculares/anormalidades
13.
J Neurophysiol ; 117(5): 1847-1852, 2017 05 01.
Artigo em Inglês | MEDLINE | ID: mdl-28250151

RESUMO

The head direction (HD) circuit is a complex interconnected network of brain regions ranging from the brain stem to the cortex. Recent work found that HD cells corecorded ipsilaterally in the anterodorsal nucleus (ADN) of the thalamus displayed coordinated firing patterns. A high-frequency oscillation pattern (130-160 Hz) was visible in the cross-correlograms of these HD cell pairs. Spectral analysis further found that the power of this oscillation was greatest at 0 ms and decreased at greater lags, and demonstrated that there was greater synchrony between HD cells with similar preferred firing directions. Here, we demonstrate that the same high-frequency synchrony exists in HD cell pairs recorded contralaterally from one another in the bilateral ADN. When we examined the cross-correlograms of HD cells that were corecorded bilaterally, we observed the same high-frequency (~150- to 200-Hz) oscillatory relationship. The strength of this synchrony was similar to the synchrony seen in ipsilateral HD cell pairs, and the degree of synchrony in each cross-correlogram was dependent on the difference in tuning between the two cells. Additionally, the frequency rate of this oscillation appeared to be independent of the firing rates of the two cross-correlated cells. Taken together, these results imply that the left and right thalamic HD network are functionally related despite an absence of direct anatomical projections. However, anatomical tracing has found that each of the lateral mammillary nuclei (LMN) project bilaterally to both of the ADN, suggesting the LMN may be responsible for the functional connectivity observed between the two ADN.NEW & NOTEWORTHY This study used bilateral recording electrodes to examine whether head direction cells recorded simultaneously in both the left and right thalamus show coordinated firing. Cross-correlations of the cells' spike trains revealed a high-frequency oscillatory pattern similar to that seen in cross-correlations between pairs of ipsilateral head direction cells, demonstrating that the bilateral thalamic head direction signals may be part of a single unified network.


Assuntos
Núcleos Anteriores do Tálamo/fisiologia , Ondas Encefálicas , Navegação Espacial , Animais , Núcleos Anteriores do Tálamo/citologia , Feminino , Lateralidade Funcional , Neurônios/fisiologia , Ratos , Ratos Long-Evans
14.
J Neurosci ; 35(6): 2547-58, 2015 Feb 11.
Artigo em Inglês | MEDLINE | ID: mdl-25673848

RESUMO

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 vestibular-associated 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.


Assuntos
Movimentos da Cabeça/fisiologia , Sistema Límbico/fisiologia , Orientação/fisiologia , Ponte/fisiologia , Animais , Comportamento Animal/fisiologia , Sinais (Psicologia) , Eletrodos Implantados , Fenômenos Eletrofisiológicos , Feminino , Sistema Límbico/citologia , Neurônios/fisiologia , Ratos , Ratos Long-Evans , Tálamo/fisiologia , Vestíbulo do Labirinto/fisiologia
15.
J Neurosci ; 35(4): 1354-67, 2015 Jan 28.
Artigo em Inglês | MEDLINE | ID: mdl-25632114

RESUMO

The neural representation of directional heading is conveyed by head direction (HD) cells located in an ascending circuit that includes projections from the lateral mammillary nuclei (LMN) to the anterodorsal thalamus (ADN) to the postsubiculum (PoS). The PoS provides return projections to LMN and ADN and is responsible for the landmark control of HD cells in ADN. However, the functional role of the PoS projection to LMN has not been tested. The present study recorded HD cells from LMN after bilateral PoS lesions to determine whether the PoS provides landmark control to LMN HD cells. After the lesion and implantation of electrodes, HD cell activity was recorded while rats navigated within a cylindrical arena containing a single visual landmark or while they navigated between familiar and novel arenas of a dual-chamber apparatus. PoS lesions disrupted the landmark control of HD cells and also disrupted the stability of the preferred firing direction of the cells in darkness. Furthermore, PoS lesions impaired the stable HD cell representation maintained by path integration mechanisms when the rat walked between familiar and novel arenas. These results suggest that visual information first gains control of the HD cell signal in the LMN, presumably via the direct PoS → LMN projection. This visual landmark information then controls HD cells throughout the HD cell circuit.


Assuntos
Movimentos da Cabeça , Cabeça , Corpos Mamilares/fisiologia , Vias Neurais/fisiologia , Orientação/fisiologia , Potenciais de Ação/efeitos dos fármacos , Potenciais de Ação/fisiologia , Análise de Variância , Animais , Sinais (Psicologia) , Agonistas de Aminoácidos Excitatórios/farmacologia , Feminino , Corpos Mamilares/citologia , Corpos Mamilares/efeitos dos fármacos , N-Metilaspartato/farmacologia , Vias Neurais/efeitos dos fármacos , Neurônios/efeitos dos fármacos , Orientação/efeitos dos fármacos , Ratos , Ratos Long-Evans
17.
J Neurophysiol ; 111(12): 2479-92, 2014 Jun 15.
Artigo em Inglês | MEDLINE | ID: mdl-24671528

RESUMO

Head direction (HD) cells respond when an animal faces a particular direction in the environment and form the basis for the animal's perceived directional heading. When an animal moves through its environment, accurate updating of the HD signal is required to reflect the current heading, but the cells still maintain a representation of HD even when the animal is motionless. This finding suggests that the HD system holds its current state in the absence of input, a view that we tested by rotating a head-restrained rat in the presence of a prominent visual landmark and then stopping it suddenly when facing the cell's preferred firing direction (PFD). Firing rates were unchanged for the first 100 ms, but then progressively decreased over the next 4 s and stabilized at ∼42% of their initial values. When the rat was stopped facing away from the PFD, there was no initial effect of braking, but the firing rate then increased steadily over 4 s and plateaued at ∼14% of its peak firing rate, substantially above initial background firing rates. In experiment 2, the rat was serially placed facing one of eight equidistant directions over 360° and held there for 30 s. Compared with the cell's peak firing rate during a passive rotation session, firing rates were reduced (51%) for in-PFD directions and increased (∼300%) from background levels for off-PFD directions, values comparable to those observed in the braking protocol. These differential HD cell responses demonstrate the importance of self-motion to the HD signal integrity.


Assuntos
Cabeça/fisiologia , Percepção de Movimento/fisiologia , Atividade Motora/fisiologia , Neurônios/fisiologia , Potenciais de Ação , Animais , Eletrodos Implantados , Comportamento Exploratório/fisiologia , Feminino , Estimulação Luminosa , Propriocepção/fisiologia , Ratos Long-Evans , Rotação
18.
J Cogn Neurosci ; 25(7): 1008-19, 2013 Jul.
Artigo em Inglês | MEDLINE | ID: mdl-23489142

RESUMO

Identifying the neural mechanisms underlying spatial orientation and navigation has long posed a challenge for researchers. Multiple approaches incorporating a variety of techniques and animal models have been used to address this issue. More recently, virtual navigation has become a popular tool for understanding navigational processes. Although combining this technique with functional imaging can provide important information on many aspects of spatial navigation, it is important to recognize some of the limitations these techniques have for gaining a complete understanding of the neural mechanisms of navigation. Foremost among these is that, when participants perform a virtual navigation task in a scanner, they are lying motionless in a supine position while viewing a video monitor. Here, we provide evidence that spatial orientation and navigation rely to a large extent on locomotion and its accompanying activation of motor, vestibular, and proprioceptive systems. Researchers should therefore consider the impact on the absence of these motion-based systems when interpreting virtual navigation/functional imaging experiments to achieve a more accurate understanding of the mechanisms underlying navigation.


Assuntos
Mapeamento Encefálico , Encéfalo/irrigação sanguínea , Encéfalo/fisiologia , Orientação , Percepção Espacial/fisiologia , Interface Usuário-Computador , Animais , Encéfalo/citologia , Humanos , Vias Neurais/irrigação sanguínea , Vias Neurais/fisiologia , Neurônios/fisiologia
19.
J Neurophysiol ; 109(3): 873-88, 2013 Feb.
Artigo em Inglês | MEDLINE | ID: mdl-23114216

RESUMO

Many species navigate in three dimensions and are required to maintain accurate orientation while moving in an Earth vertical plane. Here we explored how head direction (HD) cells in the rat anterodorsal thalamus responded when rats locomoted along a 360° spiral track that was positioned vertically within the room at the N, S, E, or W location. Animals were introduced into the vertical plane either through passive placement (experiment 1) or by allowing them to run up a 45° ramp from the floor to the vertically positioned platform (experiment 2). In both experiments HD cells maintained direction-specific firing in the vertical plane with firing properties that were indistinguishable from those recorded in the horizontal plane. Interestingly, however, the cells' preferred directions were linked to different aspects of the animal's environment and depended on how the animal transitioned into the vertical plane. When animals were passively placed onto the vertical surface, the cells switched from using the room (global cues) as a reference frame to using the vertically positioned platform (local cues) as a reference frame, independent of where the platform was located. In contrast, when animals self-locomoted into the vertical plane, the cells' preferred directions remained anchored to the three-dimensional room coordinates and their activity could be accounted for by a simple 90° rotation of the floor's horizontal coordinate system to the vertical plane. These findings highlight the important role that active movement signals play for maintaining and updating spatial orientation when moving in three dimensions.


Assuntos
Movimentos da Cabeça , Locomoção , Neurônios/fisiologia , Tálamo/fisiologia , Potenciais de Ação , Animais , Sinais (Psicologia) , Feminino , Orientação , Ratos , Ratos Long-Evans , Tálamo/citologia
20.
Hippocampus ; 23(1): 14-21, 2013 Jan.
Artigo em Inglês | MEDLINE | ID: mdl-22996337

RESUMO

A recent article by Hayman, Verriotis, Jovalekic, Fenton, and Jeffery titled Anisotropic encoding of three-dimensional space by place cells and grid cells (2011) explored how place and grid cells respond when rats locomote vertically above the ground. From their results the authors concluded a number of points about rats' abilities to orient and navigate in three dimensions. Here, we review evidence revolving around several issues including: (1) what reference frame rats use when locomoting vertically, (2) whether rats can perceive their height above the ground, (3) whether rats can estimate vertical distance and have a cognitive map in the vertical domain, (4) whether rats can path integrate in the vertical domain, and (5) does processing 3-dimensional representations require a large number of neurons. We argue that the Hayman et al. results can be accounted for by considering the reference frame the animals used in the tasks. Had the rats been facing inward with their limbs in contact with the vertical surface when moving, it is possible that different patterns of place and grid cell activity would have been observed. Further, there is good evidence to indicate that rats can orient and navigate effectively in the vertical domain.


Assuntos
Mapeamento Encefálico/métodos , Hipocampo/anatomia & histologia , Hipocampo/fisiologia , Imageamento Tridimensional/métodos , Percepção Espacial/fisiologia , Animais , Atividade Motora/fisiologia , Orientação/fisiologia , Ratos
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