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.
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.
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 otoconiadeficient 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.Key words: otolith organs; mouse; gravity; anterodorsal thalamic nucleus; navigation; head direction IntroductionAccurate navigation depends, in part, on a neural representation of directional heading, which appears to be encoded by head direction (HD) cells located throughout Papez circuit (for review, see Sharp et al., 2001a;Taube, 2007). This HD signal provides a constantly updated representation of perceived orientation in the yaw plane, regardless of the animal's position within an environment. Generation of the HD signal depends on information from the vestibular labyrinth, because damage to the vestibular labyrinth, either permanent or temporary, disrupts the HD signal and causes spatial memory impairments (Stackman and Taube, 1997;Stackman and Herbert, 2002;Wallace et al., 2002;Schautzer et al., 2003;Brandt et al., 2005). Within the vestibular labyrinth, the semicircular canals sense angular acceleration and the otolith organs sense linear acceleration, including static pitch/tilt relative to gravity (Tait and McNally, 1934;Adrian, 1943;Fernandez et al., 1972; Fernán-dez and Goldberg, 1976a,b,c). Both systems appear to be necessary for accurate perception of rotation and translation because activation of the canals occurs with respect to a head-based reference frame and the otoliths are unable to distinguish between linear acceleration and static pitch or tilt (Angelaki et al., 1999;Angelaki and Dickm...
The ability to perceive one’s position and directional heading relative to landmarks is critical 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 as critical for visual information processing. Here, we summarize the evidence that implicates the dorsal presubiculum (also known as the postsubiculum) as a critical brain structure responsible for the direct transfer of visual landmark information to spatial signals within the limbic system.
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