RESUMEN
Nearly all species rely on visual and nonvisual cues to guide navigation, and which ones they use depend on the environment and task demands. The postsubiculum (PoS) is a crucial brain region for the use of visual cues, but its role in the use of self-movement cues is less clear. We therefore evaluated rats' navigational performance on a food-carrying task in light and in darkness in rats that had bilateral neurotoxic lesions of the PoS. Animals were trained postoperatively to exit a refuge and search for a food pellet, and carry it back to the refuge for consumption. In both light and darkness, control and PoS-lesioned rats made circuitous outward journeys as they searched for food. However, only control rats were able to accurately use visual or self-movement cues to make relatively direct returns to the home refuge. These results suggest the PoS's role in navigation is not limited to the use of visual cues, but also includes the use of self-movement cues. (PsycINFO Database Record (c) 2019 APA, all rights reserved).
Asunto(s)
Hipocampo/fisiología , Fenómenos de Retorno al Lugar Habitual/fisiología , Percepción Visual/fisiología , Animales , Señales (Psicología) , Femenino , Hipocampo/metabolismo , Hipocampo/patología , Movimiento , Orientación , Ratas , Ratas Long-Evans , Percepción Espacial , Conducta Espacial , Visión Ocular/fisiologíaRESUMEN
The vestibular system provides a crucial component of place-cell and head-direction cell activity [1-7]. Otolith signals are necessary for head-direction signal stability and associated behavior [8, 9], and the head-direction signal's contribution to parahippocampal spatial representations [10-14] suggests that place cells may also require otolithic information. Here, we demonstrate that self-movement information from the otolith organs is necessary for the development of stable place fields within and across sessions. Place cells in otoconia-deficient tilted mice showed reduced spatial coherence and formed place fields that were located closer to environmental boundaries, relative to those of control mice. These differences reveal an important otolithic contribution to place-cell functioning and provide insight into the cognitive deficits associated with otolith dysfunction.
Asunto(s)
Señales (Psicología) , Hipocampo/fisiología , Movimiento (Física) , Membrana Otolítica/fisiología , Células de Lugar/fisiología , Animales , Masculino , Ratones , Movimiento/fisiologíaRESUMEN
Acetylcholine contributes to accurate performance on some navigational tasks, but details of its contribution to the underlying brain signals are not fully understood. The medial septal area provides widespread cholinergic input to various brain regions, but selective damage to medial septal cholinergic neurons generally has little effect on landmark-based navigation, or the underlying neural representations of location and directional heading in visual environments. In contrast, the loss of medial septal cholinergic neurons disrupts navigation based on path integration, but no studies have tested whether these path integration deficits are associated with disrupted head direction (HD) cell activity. Therefore, we evaluated HD cell responses to visual cue rotations in a familiar arena, and during navigation between familiar and novel arenas, after muscarinic receptor blockade with systemic atropine. Atropine treatment reduced the peak firing rate of HD cells, but failed to significantly affect other HD cell firing properties. Atropine also failed to significantly disrupt the dominant landmark control of the HD signal, even though we used a procedure that challenged this landmark control. In contrast, atropine disrupted HD cell stability during navigation between familiar and novel arenas, where path integration normally maintains a consistent HD cell signal across arenas. These results suggest that acetylcholine contributes to path integration, in part, by facilitating the use of idiothetic cues to maintain a consistent representation of directional heading. (PsycINFO Database Record
Asunto(s)
Acetilcolina/fisiología , Cabeza/fisiología , Navegación Espacial/fisiología , Acetilcolina/química , Acetilcolina/metabolismo , Animales , Derivados de Atropina/farmacología , Mapeo Encefálico/métodos , Neuronas Colinérgicas/fisiología , Señales (Psicología) , Femenino , Ratas , Ratas Long-Evans , Transducción de SeñalRESUMEN
The limbic thalamus, specifically the anterior thalamic nuclei (ATN), contains brain signals including that of head direction cells, which fire as a function of an animal's directional orientation in an environment. Recent work has suggested that this directional orientation information stemming from the ATN contributes to the generation of hippocampal and parahippocampal spatial representations, and may contribute to the establishment of unique spatial representations in radially oriented tasks such as the radial arm maze. While previous studies have shown that ATN lesions can impair spatial working memory performance in the radial maze, little work has been done to investigate spatial reference memory in a discrimination task variant. Further, while previous studies have shown that ATN lesions can impair performance in the radial maze, these studies produced the ATN lesions prior to training. It is therefore unclear whether the ATN lesions disrupted acquisition or retention of radial maze performance. Here, we tested the role of ATN signaling in a previously learned spatial discrimination task on a radial arm maze. Rats were first trained to asymptotic levels in a task in which two maze arms were consistently baited across training. After 24 h, animals received muscimol inactivation of the ATN before a 4 trial probe test. We report impairments in post-inactivation trials, suggesting that signals from the ATN modulate the use of a previously acquired spatial discrimination in the radial-arm maze. The results are discussed in relation to the thalamo-cortical limbic circuits involved in spatial information processing, with an emphasis on the head direction signal.
RESUMEN
The organization of rodent exploratory behavior appears to depend on self-movement cue processing. As of yet, however, no studies have directly examined the vestibular system's contribution to the organization of exploratory movement. The current study sequentially segmented open field behavior into progressions and stops in order to characterize differences in movement organization between control and otoconia-deficient tilted mice under conditions with and without access to visual cues. Under completely dark conditions, tilted mice exhibited similar distance traveled and stop times overall, but had significantly more circuitous progressions, larger changes in heading between progressions, and less stable clustering of home bases, relative to control mice. In light conditions, control and tilted mice were similar on all measures except for the change in heading between progressions. This pattern of results is consistent with otoconia-deficient tilted mice using visual cues to compensate for impaired self-movement cue processing. This work provides the first empirical evidence that signals from the otolithic organs mediate the organization of exploratory behavior, based on a novel assessment of spatial orientation.
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Conducta Exploratoria , Membrana Otolítica/fisiología , Animales , Señales (Psicología) , Femenino , Ratones Endogámicos C57BL , Navegación EspacialRESUMEN
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 â LMN projection. This visual landmark information then controls HD cells throughout the HD cell circuit.
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Movimientos de la Cabeza , Cabeza , Tubérculos Mamilares/fisiología , Vías Nerviosas/fisiología , Orientación/fisiología , Potenciales de Acción/efectos de los fármacos , Potenciales de Acción/fisiología , Análisis de Varianza , Animales , Señales (Psicología) , Agonistas de Aminoácidos Excitadores/farmacología , Femenino , Tubérculos Mamilares/citología , Tubérculos Mamilares/efectos de los fármacos , N-Metilaspartato/farmacología , Vías Nerviosas/efectos de los fármacos , Neuronas/efectos de los fármacos , Orientación/efectos de los fármacos , Ratas , Ratas Long-EvansRESUMEN
Navigation and the underlying brain signals are influenced by various allothetic and idiothetic cues, depending on environmental conditions and task demands. Visual landmarks typically control navigation in familiar environments but, in the absence of landmarks, self-movement cues are able to guide navigation relatively accurately. These self-movement cues include signals from the vestibular system, and may originate in the semicircular canals or otolith organs. Here, we tested the otolithic contribution to navigation on a food-hoarding task in darkness and in light. The dark test prevented the use of visual cues and thus favored the use of self-movement information, whereas the light test allowed the use of both visual and non-visual cues. In darkness, tilted mice made shorter-duration stops during the outward journey, and made more circuitous homeward journeys than control mice; heading error, trip duration, and peak error were greater for tilted mice than for controls. In light, tilted mice also showed more circuitous homeward trips, but appeared to correct for errors during the journey; heading error, trip duration, and peak error were similar between groups. These results suggest that signals from the otolith organs are necessary for accurate homing performance in mice, with the greatest contribution in non-visual environments.
Asunto(s)
Fenómenos de Retorno al Lugar Habitual/fisiología , Movimiento/fisiología , Membrana Otolítica/fisiología , Percepción Espacial/fisiología , Conducta Espacial/fisiología , Análisis de Varianza , Animales , Fenómenos Biomecánicos , Oscuridad , Ayuno/fisiología , Luz , Masculino , Ratones , Ratones Endogámicos C57BL , Ratones Mutantes , OrientaciónRESUMEN
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.
RESUMEN
The vestibular system contributes to the performance of various spatial memory tasks, but few studies have attempted to disambiguate the roles of the semicircular canals and otolith organs in this performance. This study tested the otolithic contribution to spatial working and reference memory by evaluating the performance of otoconia-deficient tilted mice on a radial arm maze and a Barnes maze. One radial arm maze task provided both intramaze and extramaze cues, whereas the other task provided only extramaze cues. The Barnes maze task provided only extramaze cues. On the radial arm maze, tilted mice performed similar to control mice when intramaze cues were available, but committed more working and reference memory errors than control mice when only extramaze cues were available. On the Barnes maze task, control and tilted mice showed similar latency, distance, and errors during acquisition training. On the subsequent probe trial, both groups spent the greatest percentage of time in the goal quadrant, indicating they were able to use extramaze cues to guide their search. Overall, these results suggest signals originating in the otolith organs contribute to spatial memory, but are not necessary for all aspects of spatial performance.
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Aprendizaje por Laberinto/fisiología , Trastornos de la Memoria/fisiopatología , Memoria/fisiología , Membrana Otolítica/fisiopatología , Percepción Espacial/fisiología , Animales , Señales (Psicología) , Discriminación en Psicología/fisiología , Masculino , Ratones Endogámicos C57BL , Ratones Transgénicos , Pruebas NeuropsicológicasRESUMEN
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.
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Mapeo Encefálico , Encéfalo/irrigación sanguínea , Encéfalo/fisiología , Orientación , Percepción Espacial/fisiología , Interfaz Usuario-Computador , Animales , Encéfalo/citología , Humanos , Vías Nerviosas/irrigación sanguínea , Vías Nerviosas/fisiología , Neuronas/fisiologíaRESUMEN
The ability to perceive one's position and directional heading relative to landmarks is necessary for successful navigation within an environment. Recent studies have shown that the visual system dominantly controls the neural representations of directional heading and location when familiar visual cues are available, and several neural circuits, or streams, have been proposed to be crucial for visual information processing. Here, we summarize the evidence that the dorsal presubiculum (also known as the postsubiculum) is critically important for the direct transfer of visual landmark information to spatial signals within the limbic system.
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Encéfalo/anatomía & histología , Encéfalo/fisiología , Orientación , Percepción Espacial/fisiología , Animales , Señales (Psicología) , HumanosRESUMEN
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.
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Encéfalo/citología , Señales (Psicología) , Movimientos de la Cabeza/fisiología , Neuronas/fisiología , Percepción Espacial/fisiología , Potenciales de Acción/fisiología , Animales , Adaptación a la Oscuridad/fisiología , Femenino , Aprendizaje por Laberinto/fisiología , Estimulación Luminosa/métodos , Ratas , Ratas Long-Evans , Análisis EspectralRESUMEN
The neural representation of directional heading is encoded by a population of cells located in a circuit that includes the postsubiculum (PoS), anterodorsal thalamus (ADN), and lateral mammillary nuclei (LMN). Throughout this circuit, many cells rely on both movement- and landmark-related information to discharge as a function of the animal's directional heading. The PoS projects to both the ADN and LMN, and these connections may convey critical spatial information about landmarks, because lesions of the PoS disrupt landmark control in head direction (HD) cells and hippocampal place cells [Goodridge and Taube (1997) J Neurosci 17:9315-9330; Calton et al. (2003) J Neurosci 23:9719-9731]. The PoS â ADN projection originates in the deep layers of PoS, but no studies have determined whether the PoS â LMN projection originates from the same cells that project to ADN. To address this issue, two distinct cholera toxin-subunit B (CTB) fluorophore conjugates (Alexa Fluor 488 and Alexa Fluor 594) were injected into the LMN and ADN of the same rats, and PoS sections were examined for cell bodies containing either or both CTB conjugates. Results indicated that the PoS â LMN projection originates exclusively from a thin layer of cells located superficial to the layer(s) of PoS â ADN projection cells, with no overlap. To verify the laminar distribution and morphological characteristics of PoS â LMN and PoS â ADN cells, biotinylated dextran amine was injected into LMN or ADN of different rats, and tissue sections were counterstained with thionin. Results indicated that the PoS â LMN projection arises from large pyramidal cells in layer IV, whereas the PoS â ADN projection arises from a heterogeneous cell population in layers V/VI. This study provides the first evidence that the PoS â ADN and PoS â LMN projections arise from distinct, nonoverlapping cell layers in PoS. Functionally, the PoS may provide landmark information to HD cells in LMN.
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Núcleos Talámicos Anteriores/fisiología , Mapeo Encefálico , Movimientos de la Cabeza/fisiología , Hipocampo/fisiología , Tubérculos Mamilares/fisiología , Células Piramidales/fisiología , Potenciales de Acción/fisiología , Animales , Femenino , Hipocampo/citología , Red Nerviosa/fisiología , Vías Nerviosas/fisiología , Orientación/fisiología , Ratas , Ratas Long-Evans , Percepción Espacial/fisiología , Corteza Visual/fisiologíaRESUMEN
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 with 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 with rats, the HD signal in mice appears to be less reliably anchored to prominent environmental cues.
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Potenciales de Acción/fisiología , Movimientos de la Cabeza/fisiología , Neuronas/fisiología , Orientación , Membrana Otolítica/fisiología , Potenciales de Acción/genética , Animales , Señales (Psicología) , Oscuridad , Proteínas de la Membrana/deficiencia , Ratones , Ratones Endogámicos C57BL , Ratones Noqueados , Membrana Otolítica/patología , Estimulación Luminosa , Ratas , Detección de Señal Psicológica/fisiología , Núcleos Talámicos/citología , Factores de TiempoRESUMEN
Hippocampal theta rhythm (HPCtheta) may be important for various phenomena, including attention and acquisition of sensory information. Two types of HPCtheta (types I and II) exist based on pharmacological, behavioral, and electrophysiological characteristics. Both types occur during locomotion, whereas only type II (atropine-sensitive) is present under urethane anesthesia. The circuit of HPCtheta synchronization includes the medial septum-diagonal band of Broca (MSDB), with cholinergic and gamma-aminobutyric acid (GABA)ergic neurons comprising the two main projections from MSDB to HPC. The primary aim of the present study was to assess the effects of GABAergic MSDB lesions on urethane- and locomotion-related HPCtheta, and compare these effects to those of cholinergic MSDB lesions. Saline, kainic acid (KA), or 192 IgG-saporin (SAP) was injected into MSDB before recording. KA preferentially destroys GABAergic MSDB neurons, whereas SAP selectively eliminates cholinergic MSDB neurons. A fixed recording electrode was placed in the dentate mid-molecular layer, and stimulating electrodes were placed in the posterior hypothalamus (PH), and medial perforant path (PP). Under urethane anesthesia, HPCtheta was induced by tail pinch, PH stimulation, and systemic physostigmine; none of the rats with KA or SAP showed HPCtheta in any of these conditions. During locomotion, HPCtheta was attenuated, but not eliminated, in rats with KA or SAP lesions. Intraseptal KA in combination with either intraseptal SAP or PP lesions reduced locomotion-related HPCtheta beyond that observed with each lesion alone, virtually eliminating HPCtheta. In contrast, intraseptal SAP combined with PP lesions did not reduce HPCtheta beyond the effect of each lesion alone. We conclude that both GABAergic and cholinergic MSDB neurons are necessary for HPCtheta under urethane, and that each of these septohippocampal projections contributes to HPCtheta during locomotion.