Maze orientation, visual and vestibular cues in two-maze spontaneous alternation of rats

Potegal, Michael; Day, Michelle; Abraham, Lawrence D.

doi:10.3758/bf03337846

Cited by 42 publications

(32 citation statements)

References 18 publications

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“…It is interesting to note that impairment of navigation in the absence of a visual cue is consistent with clinical reports of humans with bilateral vestibular dysfunction (Beritoff, 1966;Pozzo et al, 1991;Brookes et al, 1993). Together, our data and those of others (Potegal et al, 1977) indicate that vestibular-lesioned rats exhibit persistent cognitive impairments on spatial navigational tasks, which are not a consequence of a lack of attention or of locomotor deficits.…”

Section: Discussionmentioning

confidence: 49%

“…In causing similar aversive distress and disorientation symptoms, transtympanic TTX may have prevented the normal expression of place fields in the familiar cylinder environment. Although we did not test whether our TTXtreated rats were disoriented by having them perform a spatial task, other studies have shown that vestibular-lesioned rats are impaired on two different spatial tasks (Potegal et al, 1977;Ossenkopp and Hargreaves, 1993). Of course, an animal can be impaired on a spatial task without being disoriented, so these behavioral data do not provide information on the extent to which these animals were disoriented.…”

Section: Discussionmentioning

confidence: 88%

“…Repeated disorientation may have disrupted the rats' ability to form a representation of the goal location with respect to extramaze cues Martin et al, 1997). Lesions of the vestibular system impair: 1) a rat's ability to return to a goal location following passive transport (Miller et al, 1983); 2) spontaneous alternation (Potegal et al, 1977); 3) navigation in the absence of a visual landmark (Stackman and Herbert, 2002); and 4) spatial learning in a radial-arm maze task (Ossenkopp and Hargreaves, 1993). The results from studies of vestibular-lesioned animals indicate that the lesion causes deficits that are not simply a consequence of motor impairment or due to a lack of attention or motivation.…”

Section: Introductionmentioning

confidence: 99%

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Hippocampal spatial representations require vestibular input

2002

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The hippocampal formation is essential for forming declarative representations of the relationships among multiple stimuli. The rodent hippocampal formation, including the entorhinal cortex and subicular complex, is critical for spatial memory. Two classes of hippocampal neurons fire in relation to spatial features. Place cells collectively map spatial locations, with each cell firing only when the animal occupies that cell's "place field," a particular subregion of the larger environment. Head direction (HD) cells encode directional heading, with each HD cell firing when the rat's head is oriented in that cell's particular "preferred firing direction." Both landmarks and internal cues (e.g., vestibular, motor efference copy) influence place and HD cell activity. However, as is the case for navigation, landmarks are believed to exert greater influence over place and HD cell activity. Here we show that temporary inactivation of the vestibular system led to the disruption of location-specific firing in hippocampal place cells and direction-specific discharge of postsubicular HD cells, without altering motor function. Place and HD cell activity recovered over a time course similar to that of the restoration of vestibular function. These results indicate that vestibular signals provide an important influence over the expression of hippocampal spatial representations, and may explain the navigational deficits of humans with vestibular dysfunction.

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Section: Discussionmentioning

confidence: 49%

Section: Discussionmentioning

confidence: 88%

Section: Introductionmentioning

confidence: 99%

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Hippocampal spatial representations require vestibular input

2002

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“…This view necessitates a critical role for internal cue systems in spatial navigation and in the maintenance of central representations of directional heading. The present findings therefore suggest a potential neurobiological mechanism that accounts for the spatial navigational deficits observed in vestibular-lesioned humans (Beritoff, 1965;Heimbrand et al, 1991;Pozzo et al, 1991;Brookes et al, 1993) and laboratory animals (Potegal et al, 1977;Miller et al, 1983;Matthews et al, 1989;Ossenkopp and Hargreaves, 1993).…”

Section: Discussionmentioning

confidence: 92%

“…However, in the dark or when blindfolded, vestibular impaired humans show marked deficits in spatial navigation (Beritoff, 1965;Heimbrand et al, 1991;Pozzo et al, 1991;Brookes et al, 1993). Animals are known to use vestibular information to guide spatial navigation (Mittelstaedt and Mittelstaedt, 1980), and vestibular lesions disrupt performance on spatial navigation tasks (Potegal et al, 1977;Miller et al, 1983;Matthews et al, 1989;Ossenkopp and Hargreaves, 1993).…”

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confidence: 99%

Firing Properties of Head Direction Cells in the Rat Anterior Thalamic Nucleus: Dependence on Vestibular Input

1997

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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, which were unlikely to account for the loss of direction-specific firing. Vestibular lesions also disrupted the influence of angular head velocity on anterior thalamic single-unit firing rates. Finally, a subset of anterior thalamic neurons recorded from vestibularlesioned rats exhibited a pattern of intermittent firing bursts that were distinctly unrelated to HD. This novel anterior thalamic firing pattern has not been encountered in any vestibular-intact rat. These data suggest that: (1) the neural code for directional bearing is critically dependent on vestibular information; and (2) this loss of HD cell information may represent a neurobiological mechanism to account for the orientation and navigational deficits observed after vestibular dysfunction.

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Move it or lose it—Is stimulation of the vestibular system necessary for normal spatial memory?

2009

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Studies in both experimental animals and human patients have demonstrated that peripheral vestibular lesions, especially bilateral lesions, are associated with spatial memory impairment that is long-lasting and may even be permanent. Electrophysiological evidence from animals indicates that bilateral vestibular loss causes place cells and theta activity to become dysfunctional; the most recent human evidence suggests that the hippocampus may cause atrophy in patients with bilateral vestibular lesions. Taken together, these studies suggest that self-motion information provided by the vestibular system is important for the development of spatial memory by areas of the brain such as the hippocampus, and when it is lost, spatial memory is impaired. This naturally suggests the converse possibility that activation of the vestibular system may enhance memory. Surprisingly, there is some human evidence that this may be the case. This review considers the relationship between the vestibular system and memory and suggests that the evolutionary age of this primitive sensory system as well as how it detects self-motion (i.e., detection of acceleration vs. velocity) may be the reasons for its unique contribution to spatial memory.

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Maze orientation, visual and vestibular cues in two-maze spontaneous alternation of rats

Cited by 42 publications

References 18 publications

Hippocampal spatial representations require vestibular input

Hippocampal spatial representations require vestibular input

Firing Properties of Head Direction Cells in the Rat Anterior Thalamic Nucleus: Dependence on Vestibular Input

Move it or lose it—Is stimulation of the vestibular system necessary for normal spatial memory?

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