Selective hippocampal cholinergic deafferentation impairs self-movement cue use during a food hoarding task

Martin, Megan M.; Wallace, Douglas G.

doi:10.1016/j.bbr.2007.05.026

Cited by 31 publications

(26 citation statements)

References 69 publications

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“…For example, separate representations of direction and distance appear to converge on the hippocampus [49]. Accordingly, damage to the hippocampal formation [53, 54] or selective hippocampal deafferentation [55, 56] has been suggested to impair self-movement cue processing while sparing the use of environmental cues. The sequential analysis of exploratory behavior provides an alternative assessment of spatial orientation that is more acute and does not depend on food deprivation or other motivational factors.…”

Section: Discussionmentioning

confidence: 99%

Otolith dysfunction alters exploratory movement in mice

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Donaldson

et al. 2017

Behavioural Brain Research

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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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Section: Discussionmentioning

confidence: 99%

Otolith dysfunction alters exploratory movement in mice

Blankenship

Cherep

Donaldson

et al. 2017

Behavioural Brain Research

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“…Rats use environmental (i.e., visual, auditory, olfactory) and internally generated or self-movement (i.e., vestibular, proprioceptive, efferent copies of motor commands) cues to maintain spatial orientation. Immunotoxic lesions of the medial septum have been shown to spare performance on tasks in which rats can use environmental cues to guide navigation (Baxter, Gallagher 1996; McMahan et al, 1997; Cahill and Baxter, 2001; Frielingsdorf et al, 2006); whereas, impaired performance has been observed on tasks in which rats were restricted to using trial unique self-movement cues to guide navigation (Martin, Wallace, 2007). These results are consistent with a growing literature positing a role for the hippocampal formation in the online processing of self-movement cues to maintain spatial orientation (Maaswinkel et al, 1999; Wallace, Whishaw, 2003; Martin et al, 2007; for a review see Wallace et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

“…For example, dead reckoning based navigation depends on processing self-movement cues in the appropriate temporal context to estimate the direction and distance to the point where movement was initiated (Barlow, 1964; Mittelstaedt, Mittelstaedt, 1980; Etienne, 1980; Gallistel, 1990; Etienne and Jeffery, 2004; Wallace et al, 2008). Interestingly, a growing number of studies have demonstrated a role for the septohippocampal system in dead reckoning based navigation (Maaswinkel et al, 1999; Wallace, Whishaw, 2003; Martin et al, 2007; Martin, Wallace, 2007). …”

Section: Discussionmentioning

confidence: 99%

“…Therefore, spared performance may reflect the use of one source of cues to compensate for impaired processing of another set of cues. A recent study has supported this compensatory account of spared performance by examining the effects of selective MS lesions on the use of external and internal cues to guide navigation in the food hoarding paradigm (Martin, Wallace, 2007). Although rats with MS 192 IgG-saporin lesions were accurate in carrying food to a cued or hidden refuge, impairments in returning to the refuge were observed under dark conditions or when the refuge location conflicted with prior experience.…”

Section: Introductionmentioning

confidence: 99%

“…Recent work has suggested that the transition from dodging behavior to bracing behavior observed during the consumption of a food item is mediated by processes related to interval timing (Wallace et al, 2006). Separate groups of cholinergic neurons within the basal forebrain have been postulated to mediate processing external (e.g., approaching conspecific) and internally generated (e.g., interval timing) sources of information (Dunnett et al, 1991; McGaughy et al, 1996; Martin et al, 2007; Martin, Wallace, 2007). …”

Section: Introductionmentioning

confidence: 99%

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Organization of food protection behavior is differentially influenced by 192 IgG-saporin lesions of either the medial septum or the nucleus basalis magnocellularis

et al. 2008

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Converging lines of evidence have supported a role for the nucleus basalis magnocellularis (NB) in attentional mechanisms; however, debate continues regarding the role of the medial septum in behavior (MS). Recent studies have supported a role for the septohippocampal system in the online processing of internally generated cues. The current study was designed to investigate a possible double dissociation in rat food protection behavior, a natural behavior that has been shown to depend on external and internal sources of information. The study examined the effects of intraparenchymal injections of 192 IgG-saporin into either the MS or NB on the organization of food protection behavior. NB cholinergic lesions reduced the number of successful food protection behaviors while sparing the temporal organization of food protection behavior. In contrast, MS cholinergic lesions disrupted the temporal organization of food protection behavior while sparing the ability to successfully protect food items. These observations are consistent with a double dissociation of NB and MS cholinergic systems' contributions to processing external and internal sources of information and provide further evidence for the septohippocampal system's involvement in processing internally generated cues.

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Limbic system structures differentially contribute to exploratory trip organization of the rat

et al. 2012

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The role of limbic system structures in spatial orientation continues to be debated. The hippocampus (HPC) has been implicated in encoding symbolic representations of environments (i.e., cognitive map), whereas entorhinal cortex (EC) function has been implicated in self-movement cue processing (i.e., dead reckoning). These distinctions largely depend on the electrophysiological characteristics of cells within these regions and behavioral tasks that typically fail to dissociate environmental and self-movement cue processing. Topographic and kinematic characteristics of exploratory trip organization have been shown to differentially depend on environmental and self-movement cue processing. The present study examines the effects of either HPC or EC lesions on exploratory trip organization under varying lighting conditions. HPC lesions selectively impaired all measures of performance under dark conditions, but spared all measures of performance under light conditions. EC lesions impaired kinematic measures related to distance estimation under all conditions and impaired all measures of performance under light conditions. These results provide evidence that the HPC is involved in processing self-movement cues but not environmental cues, and EC is involved in processing distance estimates generated from either self-movement or environmental cues. These observations provide further support for serial processing of self-movement cues through limbic system structures that converge on the HPC.

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Selective hippocampal cholinergic deafferentation impairs self-movement cue use during a food hoarding task

Cited by 31 publications

References 69 publications

Otolith dysfunction alters exploratory movement in mice

Otolith dysfunction alters exploratory movement in mice

Organization of food protection behavior is differentially influenced by 192 IgG-saporin lesions of either the medial septum or the nucleus basalis magnocellularis

Limbic system structures differentially contribute to exploratory trip organization of the rat

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