Activity of hippocampal pyramidal neurons during trace eyeblink conditioning

Weiss, Craig; Kronforst-Collins, M. A.; Disterhoft, John F.

doi:10.1002/(sici)1098-1063(1996)6:2<192::aid-hipo9>3.0.co;2-r

Cited by 94 publications

(67 citation statements)

References 63 publications

(63 reference statements)

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“…The large responses observed in cACC during early sessions of trace EBC acquisition, but not during tests of remote retention, suggest that the cACC mediates an attentional role to enable the formation of a CS-US association by encoding behaviorally relevant stimuli (Ng et al, 2007), perhaps with feedback from the cerebellum Disterhoft, 1996, 2011;Weiss et al, 2006;Siegel and Mauk, 2013). This view is consistent with cACC lesion studies that have demonstrated impaired trace EBC acquisition (Weible et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

“…All tetrodes were then raised to the surface of the brain, and the brain was extracted out of the skull for 24 h postfixation in 10% Formalin. Subsequently, the brain was prepared for detecting marking lesions (Weiss et al, 1996). Recording sites were estimated by calculating any advancement made at the end of recording sessions with the location of the marking lesion.…”

Section: Methodsmentioning

confidence: 99%

“…A comparison of baseline firing rate and spike width was made for all the recorded neurons to distinguish pyramidal neurons from interneurons (Ranck, 1973;Weiss et al, 1996;Bruno and Simons, 2002). The population was clearly skewed toward neurons with low baseline firing rates (Fig.…”

Section: Neuronal Population and Histologymentioning

confidence: 99%

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Functional Reorganization of a Prefrontal Cortical Network Mediating Consolidation of Trace Eyeblink Conditioning

et al. 2014

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The medial prefrontal cortex (mPFC) has been studied for its role in various cognitive functions, but the roles of its subregions remain unclear. We performed tetrode recordings simultaneously from prelimbic (PL) and rostral (rACC) and caudal (cACC) anterior cingulate subregions of the rabbit mPFC to understand their interactions during learning and tests of remote memory retention for whiskersignaled trace eyeblink conditioning. cACC neurons exhibited an innate response to the conditioning stimulus (CS) that rapidly decreased across sessions, suggesting an attentional role for facilitating CS-US associations. rACC neurons from conditioned rabbits exhibited robust responses to the CS that decreased within each session, possibly evaluating its emotional salience. PL neurons exhibited robust persistent activity during the trace interval during tests of remote memory retention, suggesting its involvement in retrieval and execution of a consolidated response. Mechanistically, conditioning was associated with a greater percentage of persistently responsive neurons than neurons from pseudoconditioned control rabbits, and responses differed significantly between trials with and without conditioned responses. Collectively, these responses reflect a functional reorganization of neural activity within the prefrontal network from an attentional mode to one that orchestrates the retrieval and execution of the learned response.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Functional Reorganization of a Prefrontal Cortical Network Mediating Consolidation of Trace Eyeblink Conditioning

et al. 2014

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“…Place fields are modulated by the behavioral, cognitive, and mnemonic demands of spatial tasks, suggesting that hippocampal codes support memory guided spatial navigation (12)(13)(14)(15)(16)(17). In non-spatial memory tasks, hippocampal activity is also modulated by salient perceptual and cognitive task features independent of location, implying that the neurons may provide a global memory signal (17)(18)(19)(20)(21)(22). Indeed, hippocampal neurons respond to organizing features of experience other than spatial context by distinguishing events that occur in the same place at different times (23) or in association with different emotional significance (24,35).…”

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confidence: 99%

Motivational states activate distinct hippocampal representations to guide goal-directed behaviors

Kennedy

Shapiro²

2009

Proc. Natl. Acad. Sci. U.S.A.

154

129

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Adaptive behaviors are guided by motivation and memory. Motivational states specify goals, and memory can inform motivated behavior by providing detailed records of past experiences when goals were obtained. These 2 fundamental processes interact to guide animals to biologically relevant targets, but the neuronal mechanisms that integrate them remain unknown. To investigate these mechanisms, we recorded unit activity from the same population of hippocampal neurons as rats performed identical tasks while either food or water deprived. We compared the influence of motivational state (hunger and thirst), memory demand, and spatial behavior in 2 tasks: hippocampus-dependent contextual memory retrieval and hippocampus-independent random foraging. We found that: (i) hippocampal coding was most strongly influenced by motivational state during contextual memory retrieval, when motivational cues were required to select among remembered, goal-directed actions in the same places; (ii) the same neuronal populations were relatively unaffected by motivational state during random foraging, when hunger and thirst were incidental to behavior, and signals derived from deprivation states thus informed, but did not determine, hippocampal coding; and (iii) ''prospective coding'' in the contextual retrieval task was not influenced by allocentric spatial trajectory, but rather by the animal's deprivation state and the associated, nonspatial target, suggesting that hippocampal coding includes a wide range of predictive associations. The results show that beyond coding spatiotemporal context, hippocampal representations encode the relationships between internal states, the external environment, and action to provide a mechanism by which motivation and memory are coordinated to guide behavior.hippocampus ͉ memory ͉ neuronal coding E pisodic memory provides a record of past experience and is structured by spatial, temporal, and personal contexts (1), multiple frames of reference that organize the features of events and provide global categories for information storage and retrieval. Motivational states arising from interoceptive cues provide an internal context that modulates the relative significance, meaning, or organization of events in memory (2, 3). Thus, motivational states such as hunger and thirst define internal, contextual cues that can specify behavioral goals and inform memory retrieval.The hippocampus is required for episodic memory in humans (4, 5) and episodic-like memory in other animals (6). Hippocampal neurons typically fire in place fields, local regions of an environment that selectively elicit significant activity (7). Place field properties suggest that the hippocampus helps code the animal's location within spatial contexts (7-11). Place fields are modulated by the behavioral, cognitive, and mnemonic demands of spatial tasks, suggesting that hippocampal codes support memory guided spatial navigation (12-17). In non-spatial memory tasks, hippocampal activity is also modulated by salient perceptual and cognitive task ...

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“…No such pattern of volume change was observed in V1 during delay conditioning, although this region did exhibit an increase in BOLD response magnitude that persisted throughout both stages of training, as well as CS-alone memory trials. Similarly, robust neuronal responses have been observed in the hippocampus during delay conditioning (Berger et al, 1983), and the responses were greater in terms of amplitude and duration during delay than during trace conditioning (Weiss et al, 1996) even though this region, like V1, is not required for acquisition of the paradigm.…”

Section: Discussionmentioning

confidence: 71%

Functional Magnetic Resonance Imaging of Delay and Trace Eyeblink Conditioning in the Primary Visual Cortex of the Rabbit

Miller

Weiss²,

Song

et al. 2008

J. Neurosci.

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The primary sensory cortices have been shown in recent years to undergo experience-and learning-related plasticity under a variety of experimental circumstances. In this study, we used functional magnetic resonance imaging (fMRI) in parallel with both delay and trace eyeblink conditioning to image the learning-related functional activation within the primary visual cortex (V1) of awake, behaving rabbits. We expected that the differing level of forebrain dependence between these two conditioning paradigms should produce a differential blood oxygenation level-dependent (BOLD) functional response in V1. Our results showed a significant expansion of activated volume within V1, particularly early in learning, after training with the more cognitively demanding trace paradigm. In contrast, the simpler delay paradigm produced an increase in the magnitude of the BOLD response in activated voxels, but no significant change in activated volume. No accompanying learning-related changes were observed in the primary somatosensory cortex, which mediates the unconditioned stimulus. These results suggest that the recruitment of additional neurons within V1 is necessary to support the more demanding memory imposed by the trace interval. To our knowledge, this work is the first functional imaging study to compare directly trace and delay eyeblink conditioning in an animal model.

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Activity of hippocampal pyramidal neurons during trace eyeblink conditioning

Cited by 94 publications

References 63 publications

Functional Reorganization of a Prefrontal Cortical Network Mediating Consolidation of Trace Eyeblink Conditioning

Functional Reorganization of a Prefrontal Cortical Network Mediating Consolidation of Trace Eyeblink Conditioning

Motivational states activate distinct hippocampal representations to guide goal-directed behaviors

Functional Magnetic Resonance Imaging of Delay and Trace Eyeblink Conditioning in the Primary Visual Cortex of the Rabbit

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