A minimal synaptic architecture is proposed for how the brain might perform path integration by computing the next internal representation of self-location from the current representation and from the perceived velocity of motion. In the model, a place-cell assembly called a “chart ” contains a twodimensional attractor set called an “attractor map ” that can be used to represent coordinates in any arbitrary environment, once associative binding has occurred between chart locations and sensory inputs. In hippocampus, there are different spatial relations among place fields in different environments and behavioral contexts. Thus, the same units may participate in many charts, and it is shown that the number of uncorrelated charts that can be encoded in the same recurrent network is potentially quite large. According to this theory, the firing of a given place cell is primarily a cooperative effect of the activity of its

The head-direction (HD) cells found in the limbic system in freely moving rats represent the instantaneous head direction of the animal in the horizontal plane regardless of the location of the animal. The internal direction represented by these cells uses both self-motion information for inet-tially based updating and familiar visual landmarks for calibration. Here, a model of the dynamics of the HD cell ensemble is presented. The sta-bility of a localized static activity profile in the network and a dynamic shift mechanism are explained naturally by synaptic weight distribution components with even and odd symmetry, respectively. Under symmetric weights or symmetric reciprocal connections, a stable activity profile close to the known direc-tional tuning curves will emerge. By adding a slight asymmetry to the weights, the activity profile will shift continuously without 1

Previous studies have shown that hippocampal place fields are controlled by the salient sensory cues in the environ-ment, in that rotation of the cues causes an equal rotation of the place fields. We trained rats to forage for food pellets in a gray cylinder with a single salient directional cue, a white card covering 90 ” of the cylinder wall. Half of the rats were disoriented before being placed in the cylinder, in or-der to disrupt their internal sense of direction. The other half were not disoriented before being placed in the cylin-der; for these rats, there was presumably a consistent re-lationship between the cue card and their internal direction sense. We subsequently recorded hippocampal place cells and thalamic head direction cells from both groups of rats as they moved in the cylinder; between some sessions the cylinder and cue card were rotated to a new direction. All

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

Place cells of the hippocampal formation encode a spatial representation of the environment, and the orientation of this representation is apparently governed by the head direction cell system. The representation of a well explored environment by CA1 place cells can be split when there is conflicting information from salient proximal and distal cues, because some place fields rotate to follow the distal cues, whereas others rotate to follow the proximal cues (Knierim, 2002a). In contrast, the CA3 representation is more coherent than CA1, because the place fields in CA3 tend to rotate in the same direction (Lee et al., 2004). The present study tests whether the head direction cell network produces a split representation or remains coherent under these conditions by simultaneously recording both CA1 place cells and head direction cells from the thalamus. In agreement with previous studies, split representations of the environment were observed in ensembles of CA1 place cells in �75 % of the mismatch sessions, in which some fields followed the counterclockwise rotation of proximal cues and other fields followed the clockwise rotation of distal cues. However, of 225 recording sessions, there was not a single instance of the head direction cell ensembles revealing a split representation of head direction. Instead, in most of the mismatch sessions, the head direction cell tuning curves rotated as an ensemble clockwise (94%) and in a few sessions rotated counterclockwise (6%). The findings support the notion that the head direction cells may be part of an attractor network bound more strongly to distal landmarks than proximal landmarks, even under conditions in which the CA1 place representation loses its coherence. Key words: place cells; head direction cells; ensemble recording; attractor neural network; spatial orientation; single units

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firing rates of anterodorsal thalamic head direction cells. J Neurophysiol 86: 692–702, 2001. Head direction (HD) cells discharge selectively in macaques, rats, and mice when they orient their head in a specific (“preferred”) direction. Preferred directions are influenced by visual cues as well as idiothetic self-motion cues derived from vestibular, proprioceptive, motor efferent copy, and command signals. To distinguish the relative importance of active locomotor signals, we compared HD cell response properties in 49 anterodorsal thalamic HD cells of six male Long-Evans rats during active displacements in a foraging task as well as during passive rotations. Since thalamic HD cells typically stop firing if the animals are tightly restrained, the rats were trained to remain immobile while drinking water distributed at intervals from a small reservoir at the center of a rotatable platform. The platform was rotated in a clockwise/counterclockwise oscillation to record directional responses in the stationary animals while the surrounding environmental cues remained stable. The peak rate of directional firing decreased by 27 % on average during passive rotations (r 2 � 0.73, P � 0.001). Individual cells recorded in sequential sessions (n � 8) reliably showed comparable reductions in peak firing, but simultaneously recorded cells did not necessarily produce identical responses. All of the HD cells maintained the same preferred directions during passive rotations. These results are consistent with the hypothesis that the level of locomotor activity provides a statedependent modulation of the response magnitude of AD HD cells. This could result from diffusely projecting neuromodulatory systems associated with motor state.

ABSTRACT: This study investigated location-, movement-, and directional-selectivity of action potential discharges of hippocampal neurons in awake rats subjected to passive displacements in order to estimate vestibular contributions to this activity. Water-deprived rats were habituated to being restrained in a sling mounted on a moving robot. The extracellular activity of single complex-spike cells in area CA1 of the hippocampus was recorded with glass micropipettes in the rats during passive translations, rotations, and immobility. The robot made a standardized series of trajectories starting from each of four corners of a square enclosure surrounded by black curtains. A drop of water was delivered to the rat each time the robot arrived at one designated corner of the arena. The activities of 29 neurons were investigated in 45 recording sessions (16 of which were in total darkness) in four rats. Hippocampal neurons recorded in 31 sessions (9 sessions in the dark) had significant locationselective increases or decreases in firing rate as the rat was passively

Two populations of limbic neurons are likely neurophysiological substrates for cognitive operations required for spatial orientation and navigation: hippocampal pyramidal cells discharge selectively when the animal is in a certain place (the “firing field”) in the environment, whereas head direction cells discharge when the animal orients its head in a specific, “preferred” direction. Cressant et al. (1997) showed that the firing fields of hippocampal place cells reorient relative to a group of three-dimensional objects only if these are at the periphery, but not the center of an enclosed platform. To test for corresponding responses in head direction cells, three objects were equally spaced along the periphery of a circular platform. Preferred directions were measured before and after the group of objects was rotated. (The rat was disoriented in total darkness between sessions). This was repeated in the presence or absence of a cylinder enclosing the platform. When the enclosure was present, the preferred directions of all 30 cells recorded shifted by the same angle as the objects. In the absence of the enclosure, the preferred directions did not follow the objects, remaining fixed relative to the room. These results provide a possible neurophysiological basis for observations from psychophysical experiments in humans that background, rather than foreground, cues are preferentially used for spatial orientation. Key words: foreground; background; landmark; spatial orientation; place cells; navigation In monkeys, rats, and mice, two types of limbic system neurons have been observed that may function as neurophysiological substrates for spatial orientation. Hippocampal neurons discharge selectively when the animal is at a certain location in the environment (the firing field of the “place ” cell; O’Keefe and Conway,