Lesions of the Tegmentomammillary Circuit in the Head Direction System Disrupt the Head Direction Signal in the Anterior Thalamus

Bassett, Joshua P.; Tullman, Matthew L.; Taube, Jeffrey S.

doi:10.1523/jneurosci.0268-07.2007

Cited by 115 publications

(135 citation statements)

References 55 publications

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“…The dorsal nucleus of Gudden is thought to be necessary for generating the head-direction signal (e.g., Bassett et al, 2007) and, hence, is required for tasks that require path integration (Frohardt et al, 2006). Despite the consensus that head-direction information is integral for effective navigation and the potential use of directional information to solve some of the present spatial tasks (Hamilton et al, 2008), lesions of the lateral mammillary body, which block head-direction information (e.g., Blair et al, 1998), have only mild effects on the tasks used in the present study (Vann, 2005).…”

Section: Discussionmentioning

confidence: 99%

Selective disconnection of the hippocampal formation projections to the mammillary bodies produces only mild deficits on spatial memory tasks: Implications for fornix function

et al. 2011

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ABSTRACT:It is now clear that the integrity of the fornix is important for normal mnemonic function. The fornix, however, is a major white matter tract, carrying numerous hippocampal formation afferents and efferents, and it is not known which specific components support memory processes. Established theories of extended hippocampal function emphasize the sequential pathway from the hippocampal formation (i.e., subicular complex) to the mammillary bodies and, thence, to the anterior thalamus, as pathology in each of these structures is implicated in anterograde amnesia in humans and spatial memory deficits in rats. The specific importance of the hippocampal formation projections that just innervate the mammillary bodies has, however, never been tested. This study isolated these specific projections in the rat by selectively cutting the descending component of the postcommissural fornix. Two successive, cohorts of rats with these tract lesions were tested on working memory tasks in the water-maze, T-maze, and radial-arm maze. Disconnecting the descending postcommissural fornix had only a mild effect or sometimes no apparent effect on the performance of these spatial memory tasks, even though tracing experiments confirmed the loss of hippocampal formation-mammillary projections. One implication is that the spatial deficits found in rats following standard fornix lesions are only partly attributable to the loss of projections from the hippocampal formation to the mammillary bodies. Perhaps more surprising, the behavioral impact of cutting the descending postcommissural fornix in rats appeared appreciably less than the effect of either mammillary body or mammillothalamic tract lesions. The present experiments show that the mammillary bodies can still effectively support spatial memory in the absence of their dense subicular complex inputs, so revealing the importance of the other afferents for sustaining mammillary body function. This new evidence for independent functions shows that the mammillary bodies are more than just a hippocampal relay. V V C 2010 Wiley-Liss, Inc.

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Section: Discussionmentioning

confidence: 99%

Selective disconnection of the hippocampal formation projections to the mammillary bodies produces only mild deficits on spatial memory tasks: Implications for fornix function

et al. 2011

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“…Theta-bursting cells are found throughout the hippocampal circuitry, but evidence indicates that the theta rhythm originates within subcortical structures such as the raphe nuclei and mammillary bodies (for review, see Vertes and Kocsis, 1997;Vertes et al, 2001;Pan and McNaughton, 2004;Sharp and Koester, 2008), immediately adjacent to structures where ring attractors for angular path integration by head-direction cells are thought to reside (Blair et al, 1998;Sharp et al, 2001a,b;Basset et al, 2007). These subcortical areas are well positioned to receive ascending input from the vestibular and motor systems, which could encode the velocity signals that must be integrated to generate the position signal.…”

Section: Ring Attractor Model Of the Velocity-modulated Theta Oscillatormentioning

confidence: 99%

Conversion of a phase‐ to a rate‐coded position signal by a three‐stage model of theta cells, grid cells, and place cells

2008

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ABSTRACT:As a rat navigates through a familiar environment, its position in space is encoded by firing rates of place cells and grid cells. Oscillatory interference models propose that this positional firing rate code is derived from a phase code, which stores the rat's position as a pattern of phase angles between velocity-modulated theta oscillations. Here we describe a three-stage network model, which formalizes the computational steps that are necessary for converting phase-coded position signals (represented by theta oscillations) into rate-coded position signals (represented by grid cells and place cells). The first stage of the model proposes that the phase-coded position signal is stored and updated by a bank of ring attractors, like those that have previously been hypothesized to perform angular path integration in the head-direction cell system. We show analytically how ring attractors can serve as central pattern generators for producing velocity-modulated theta oscillations, and we propose that such ring attractors may reside in subcortical areas where hippocampal theta rhythm is known to originate. In the second stage of the model, grid fields are formed by oscillatory interference between theta cells residing in different (but not the same) ring attractors. The model's third stage assumes that hippocampal neurons generate Gaussian place fields by computing weighted sums of inputs from a basis set of many grid fields. Here we show that under this assumption, the spatial frequency spectrum of the Gaussian place field defines the vertex spacings of grid cells that must provide input to the place cell. This analysis generates a testable prediction that grid cells with large vertex spacings should send projections to the entire hippocampus, whereas grid cells with smaller vertex spacings may project more selectively to the dorsal hippocampus, where place fields are smallest. V

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“…Standard electrophysiological studies in juvenile animals will reveal whether grid cell responses develop pre-or post-natally, and if they develop postnatally, such studies will elucidate the dynamics of learning and plasticity in dMEC. Lesion studies that can reversibly inactivate rhythm-producing inputs and regions of the hippocampal formation in adult and juvenile animals may begin to probe whether oscillations are necessary for grid cell dynamics or establishment, respectively (Vertes and Kocsis, 1997;Vertes et al, 2001;Pan and McNaughton, 2004;Bassett et al, 2007;. Cortex cooling (Lomber et al, 1999) or pharmacological interventions (Liu et al, 2007) which reduce the efficacy of recurrent connections in superficial cortical layers without greatly affecting the efficacy of feed-forward inputs, could help to determine the importance and functional role of recurrent connectivity in the generation of grid responses.…”

Section: Open Questionsmentioning

confidence: 99%

Grid cells: The position code, neural network models of activity, and the problem of learning

2008

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ABSTRACT:We review progress on the modeling and theoretical fronts in the quest to unravel the computational properties of the grid cell code and to explain the mechanisms underlying grid cell dynamics. The goals of the review are to outline a coherent framework for understanding the dynamics of grid cells and their representation of space; to critically present and draw contrasts between recurrent network models of grid cells based on continuous attractor dynamics and independentneuron models based on temporal interference; and to suggest open questions for experiment and theory. V

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Lesions of the Tegmentomammillary Circuit in the Head Direction System Disrupt the Head Direction Signal in the Anterior Thalamus

Cited by 115 publications

References 55 publications

Selective disconnection of the hippocampal formation projections to the mammillary bodies produces only mild deficits on spatial memory tasks: Implications for fornix function

Selective disconnection of the hippocampal formation projections to the mammillary bodies produces only mild deficits on spatial memory tasks: Implications for fornix function

Conversion of a phase‐ to a rate‐coded position signal by a three‐stage model of theta cells, grid cells, and place cells

Grid cells: The position code, neural network models of activity, and the problem of learning

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