A description of the amygdalo-hippocampal interconnections in the macaque monkey

Aggleton, John Patrick

doi:10.1007/bf00340489

Cited by 148 publications

(103 citation statements)

References 27 publications

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“…These observations are congruent with previous findings that amygdalar lesions block or attenuate a range of stress-induced effects such as LTP and spatial memory , gastric erosion (Henke, 1981), and analgesia (Helmstetter, 1992). Anatomically, the amygdala sends direct (from the magnocellular and parvicellular divisions of the basolateral amygdala to the CA1 and subiculum) and indirect (via the entorhinal cortex) projections to the hippocampus (Krettek and Price, 1977;Aggleton, 1986;Pikkarainen et al, 1999), routes by which it can influence hippocampal functions (Kim and Diamond, 2002). Because muscimol increases Cl Ϫ ion conductance across cell membranes (Feldman et al, 1997), the drug effects presumably are caused by inhibition of amygdalo-hippocampal activity during stress.…”

Section: Discussionsupporting

confidence: 91%

Amygdalar Inactivation Blocks Stress-Induced Impairments in Hippocampal Long-Term Potentiation and Spatial Memory

Kim¹,

Koo²,

Lee³

et al. 2005

J. Neurosci.

167

145

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Electrolytic lesions to the amygdala, a limbic structure implicated in stress-related behaviors and memory modulation, have been shown to prevent stress-induced impairments of hippocampal long-term potentiation (LTP) and spatial memory in rats. The present study investigated the role of intrinsic amygdalar neurons in mediating stress effects on the hippocampus by microinfusing the GABA A receptor agonist muscimol into the amygdala and examining stress effects on Schaffer collateral/commissural-CA1 LTP and spatial memory. The critical period of the amygdalar contribution to stress effects on hippocampal functions was determined by applying muscimol either before stress or immediately after stress. Our results indicate that intra-amygdalar muscimol infusions before uncontrollable restrainttailshock stress effectively blocked stress-induced physiological and behavioral effects. Specifically, hippocampal slices prepared from vehicle-infused stressed animals exhibited markedly impaired LTP, whereas slices obtained from muscimol-infused stressed animals demonstrated robust LTP comparable with that of unstressed animals. Correspondingly, vehicle-infused stressed animals displayed impaired spatial memory (on a hidden platform version of the Morris water maze task), whereas muscimol-infused stressed animals revealed unimpaired spatial memory. In contrast to prestress muscimol effects, however, immediate poststress infusions of muscimol into the amygdala failed to interfere with stress impairments of LTP and spatial memory. Together, these results suggest that the amygdalar neuronal activity during stress, but not shortly after stress, is essential for the emergence of stress-induced alterations in hippocampal LTP and memory.

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Section: Discussionsupporting

confidence: 91%

Amygdalar Inactivation Blocks Stress-Induced Impairments in Hippocampal Long-Term Potentiation and Spatial Memory

Kim¹,

Koo²,

Lee³

et al. 2005

J. Neurosci.

167

145

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“…The hippocampus can modulate the CS and US inputs via projections to the pontine nucleus and the dorsal accessory olive (Berger et al, 1986;Steinmetz et al, 1988;Schmajuk and DiCarlo, 1992). In addition, the amygdala projects to the hippocampal formation, including a CA1 area, the subiculum, and the entorhinal cortex (Krettek and Price, 1977;Aggleton, 1986). The present findings suggest that the projection from the amygdala to the cerebellum (e.g., via the lateral tegmental field) normally exerts an excitatory influence on the acquisition of eyeblink CRs (Fig.…”

Section: Discussionmentioning

confidence: 53%

Differential Effects of Cerebellar, Amygdalar, and Hippocampal Lesions on Classical Eyeblink Conditioning in Rats

Lee¹,

Kim²

2004

J. Neurosci.

133

150

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Eyeblink conditioning has been hypothesized to engage two successive stages of nonspecific emotional (fear) and specific musculature (eyelid) learning, during which the nonspecific component influences the acquisition of the specific component. Here we test this notion by investigating the relative contributions of the cerebellum, the amygdala, and the hippocampus to the emergence of conditioned eyelid and fear responses during delay eyeblink conditioning in freely moving rats. Periorbital electromyography (EMG) and 22 kHz ultrasonic vocalization (USV) activities were measured concurrently from the same subjects and served as indices of conditioned eyeblink and fear responses, respectively. In control animals, conditioned EMG responses increased across training sessions, whereas USV responses were initially robust but decreased across training sessions. Animals with electrolytic lesions to their cerebellum (targeting the interpositus nucleus) were completely unable to acquire conditioned EMG responses but exhibited normal USV behavior, whereas animals with lesions to the amygdala showed decelerated acquisition of conditioned EMG responses and displayed practically no USV behavior. In contrast, hippocampal lesioned rats demonstrated facilitated acquisition of conditioned EMG responses, whereas the USV behavior was unaffected. The amygdalar involvement in eyeblink conditioning was examined further by applying the GABA A agonist muscimol directly into the amygdala either before or immediately after training sessions. Although pretraining muscimol infusions impaired conditioned EMG responses, post-training infusions did not. Together, these results suggest that, even during a simple delay eyeblink conditioning, animals learn about different aspects associated with the behavioral task that are subserved by multiple brain-memory systems that interact to produce the overall behavior.

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“…Indeed, output connectivity of the primate hippocampus with subcortical areas -including nucleus accumbens 173 -follows a graded topography similar to that in rodents 174 (but note longitudinally restricted vs. distributed hippocampal-amygdala projections in primates and rodents, respectively 107,175 ). Input connectivity from entorhinal cortex to DG also follow a graded mapping that is analogous to that in rats [34][35] , with an anteromedial-posterolateral EC axis corresponding to an anterior-posterior DG termination [176][177][178] .…”

Section: Box 1 Is the Rodent Ventral-dorsal Axis Homologous To The Pmentioning

confidence: 94%

Functional organization of the hippocampal longitudinal axis

Witter²,

et al. 2014

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The precise functional role of the hippocampus remains a topic of much debate. According to a dominant view, the dorsal/posterior hippocampus is implicated in memory and spatial navigation and the ventral/anterior hippocampus mediates anxietyrelated behaviours. However, this 'dichotomy view' may need revision. Gene expression studies demonstrate multiple functional domains along the hippocampal long axis, which often exhibit sharply demarcated borders. By contrast, anatomical studies and electrophysiological recordings in rodents suggest that the long-axis is organized along a gradient. Together, these observations suggest a model in which functional long-axis gradients are superimposed on discrete functional domains. This model provides a potential framework to explain and test the multiple functions ascribed to the hippocampus.The hippocampus is a medial temporal lobe structure critically involved in episodic memory and spatial navigation [1][2][3][4][5][6][7] . Its long, curved form is present across all mammalian orders and runs along a dorsal (septal) to ventral (temporal) axis in rodents, corresponding to a posteriorto-anterior axis in humans (FIG. 1a-b). The same basic intrinsic circuitry is maintained throughout the long axis and across species (FIG. 1c). Despite this conserved intrinsic circuitry, the dorsal and ventral portions have different connectivities with cortical and subcortical areas, and this has long posed a question as to whether the hippocampus is functionally uniform along this axis. Here we review cross-species data that show how the seemingly disparate functions ascribed to the hippocampus can be accommodated by a model in which different functional properties exist along the longitudinal axis.The severe memory impairment suffered by patient H.M. following bilateral hippocampal resection 1 led to intensive study 8 of patients and animal models with hippocampal damage, with an ensuing characterisation of hippocampal function in terms of declarative memory 2 , encompassing both episodic and semantic memory. At the same time, however, evidence emerged for a hippocampal role in spatial memory, based on the discovery of hippocampal 'place cells' 9,10 and the demonstration that hippocampal lesions impair spatial memory 4 . Both the declarative memory hypothesis 11 and the spatial mapping hypothesis 12 of hippocampal function proposed a unitary model in which the entire hippocampus is dedicated

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A description of the amygdalo-hippocampal interconnections in the macaque monkey

Cited by 148 publications

References 27 publications

Amygdalar Inactivation Blocks Stress-Induced Impairments in Hippocampal Long-Term Potentiation and Spatial Memory

Amygdalar Inactivation Blocks Stress-Induced Impairments in Hippocampal Long-Term Potentiation and Spatial Memory

Differential Effects of Cerebellar, Amygdalar, and Hippocampal Lesions on Classical Eyeblink Conditioning in Rats

Functional organization of the hippocampal longitudinal axis

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