Contribution of hippocampal place cell activity to learning and formation of goal-directed navigation in rats

Kobayashi, T; Tran, Anh T.; Nishijo, Hisao; Ono, Taketoshi; Matsumoto, Gen

doi:10.1016/s0306-4522(02)00700-5

Cited by 64 publications

(61 citation statements)

References 60 publications

(76 reference statements)

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“…Previously, Deadwyler et al (1996) made a similar proposal based on an analysis of the activity of small populations of hippocampal cells in rats solving a delayed-matching-to-sample task. Finally, Kobayashi et al (2003) recorded place cells from rats trained to take fixed trajectories to obtain intracranial stimulation rewards at two specific locations in a cylinder. They found that some cells changed their firing patterns as the rat learned the task and displayed excess firing at the two rewarded locations.…”

Section: Discussionmentioning

confidence: 99%

“…For example, firing fields do not tend to occur in higher numbers near goal locations (Lenck-Santini et al, 2001, 2002 and do not seem to undergo systematic changes when the goal is moved (Speakman and O'Keefe, 1990;Trullier et al, 1999;Lenck-Santini et al, 2001). In contrast, there have been several reports that firing fields occur in excess at goal locations (Gothard et al, 1996;Hollup et al, 2001;Hölscher et al, 2003;Kobayashi et al, 2003).…”

Section: Introductionmentioning

confidence: 91%

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Goal-Related Activity in Hippocampal Place Cells

Hok¹,

Lenck-Santini²,

Roux³

et al. 2007

J. Neurosci.

210

182

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Place cells are hippocampal neurons whose discharge is strongly related to a rat's location in its environment. The existence of place cells has led to the proposal that they are part of an integrated neural system dedicated to spatial navigation, an idea supported by the discovery of strong relationships between place cell activity and spatial problem solving. To further understand such relationships, we examined the discharge of place cells recorded while rats solved a place navigation task. We report that, in addition to having widely distributed firing fields, place cells also discharge selectively while the hungry rat waits in an unmarked goal location to release a food pellet. Such firing is not duplicated in other locations outside the main firing field even when the rat's behavior is constrained to be extremely similar to the behavior at the goal. We therefore propose that place cells provide both a geometric representation of the current environment and a reflection of the rat's expectancy that it is located correctly at the goal. This on-line feedback about a critical aspect of navigational performance is proposed to be signaled by the synchronous activity of the large fraction of place cells active at the goal. In combination with other (prefrontal) cells that provide coarse encoding of goal location, hippocampal place cells may therefore participate in a neural network allowing the rat to plan accurate trajectories in space.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 91%

Goal-Related Activity in Hippocampal Place Cells

Hok¹,

Lenck-Santini²,

Roux³

et al. 2007

J. Neurosci.

210

182

View full text Add to dashboard Cite

show abstract

“…Enhanced Arc mRNA expression could reflect increased firing of neurons that express information retrieved from memory in their goal-directed activity and thus represent memory traces (Wood et al, 2000;Hollup et al, 2001;Fyhn et al, 2002;Nakazawa et al, 2003;Kobayashi et al, 2003). It is thought that HC place cells and head direction cells found in CA1, postsubiculum, anterior dorsal thalamus, and lateral mammillary nuclei are interacting parts of the rodent navigational system (Leutgeb et al, 2000;Calton et al, 2003) that rely on allocentric and idiothetic information processing (Eichenbaum et al, 1990;Whishaw and Maaswinkel, 1998).…”

Section: Discussionmentioning

confidence: 99%

Topography of Arc/Arg3.1 mRNA Expression in the Dorsal and Ventral Hippocampus Induced by Recent and Remote Spatial Memory Recall: Dissociation of CA3 and CA1 Activation

Gusev¹,

Cui²,

Alkon³

et al. 2005

J. Neurosci.

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The understanding of the mechanisms of memory retrieval and its deficits, and the detection of memory underlying neuronal plasticity, is greatly impeded by a lack of precise knowledge of the brain circuitry that underlies the functions of memory. The specific roles of anatomically distinct hippocampal subdivisions in recent and long-term memory retention and recall are essentially unknown. To address these questions, we mapped the expression of Arc/Arg 3.1 mRNA, a neuronal activity marker, in memory retention at multiple rostrocaudal levels of the dentate gyrus, CA3, CA1, subiculum, and lateral and medial entorhinal cortices after a platform search in a water-maze spatial task at 24 h and 1 month compared with swim and naive controls. We found that the entorhinohippocampal neuronal activity underlying the recall of recent and remote spatial memory has an anatomically distributed and time-dependent organization throughout both the dorsal and ventral hippocampus that is subdivision specific. We found a dissociation in the activity of the entorhinal cortex, CA3, and CA1 over a period of memory consolidation. Although CA3, the dorsal hippocampus, and the entorhinal cortex demonstrated the most persistent learning-specific signal during both recent and long-term memory recall, CA1 and the ventral hippocampus displayed the most dramatic signal decline. We determined the coordinates of activity clusters in the hippocampal subdivisions during the platform search and their dynamics over time. Our mapping data suggest that although the level of corticohippocampal interaction is similar during the retrieval of recent and remote spatial memories, the mnemonic function of the hippocampus may have changed, and the activity underlying remote spatial memory could be anatomically segregated within hippocampal subdivisions in small segments.

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“…The mesolimbic and mesocortical pathways, arising mainly from the ventral tegmental area and innervating the mesial parts of the limbic system, including the NAc, AM, HF, and prefrontal cortex, function in incentive motivational processes (1,(7)(8)(9). It has been reported that reward information is processed in the prefrontal cortex, AM, and ventral tegmental area (3,(23)(24)(25)(26)(27)(28), and spatial information is processed in the HF (5,29,30), both of which then converge on NAc neurons (10,11,15,19). The D1R-KO eliminated the prereward excitatory response in the NAc of mice, whereas the response during and after reward was unchanged.…”

Section: Discussionmentioning

confidence: 99%

Dopamine D1 receptors involved in locomotor activity and accumbens neural responses to prediction of reward associated with place

Tran

Tamura²,

Uwano³

et al. 2005

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

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Predicting reward is essential in learning approach behaviors. Dopaminergic activity has been implicated in reward, movement, and cognitive processes, all essential elements in learning. The nucleus accumbens (NAc) receives converging inputs from corticolimbic information-processing areas and from mesolimbic dopamine neurons originating in the ventral tegmental area. Previously, we reported that in mice, a dopamine D2 receptor knockout (D2R-KO) eliminated the prereward inhibitory response, increased place-field size of NAc neurons, and reduced locomotor activity without marked change in intracranial self-stimulation (ICSS) behavior. The present study investigated the specific contribution of dopamine D1 receptor (D1R) in mediating reward, locomotor activity, and spatial associative processes and in regulating NAc neural responses. In contrast to D2R-KO animals, here we find D1R-KO in mice selectively eliminated the prereward excitatory response and decreased place-field size of NAc neurons. Furthermore, D1R-KO impaired ICSS behavior, seriously reduced locomotor activity, and retarded acquisition of a place learning task. Thus, the present results suggest that D1R may be an important determinant in brain stimulation reward (ICSS) and participates in coding for a type of reward prediction of NAc neurons and in spatial learning.dopamine receptor ͉ nucleus accumbens ͉ spatial learning D opaminergic systems innervate the hippocampal formation (HF), prefrontal cortex, amygdala (AM), and ventral striatum and mediate cognitive processes of working memory and learning (1-6). The nucleus accumbens (NAc) is reliably linked to motivation, locomotion, reward-related processes, and some cognitive functions (1,3,(7)(8)(9). It receives excitatory glutamatergic input from the prefrontal cortex, HF, and AM, as well as a dense converging dopaminergic innervation from the ventral tegmental area (3, 10, 11). Thus, NAc neurons are positioned to recognize context-driven patterns of activation and to relay this information to planning and motor executive systems for appropriate behavioral responses (1,3,7,8,12). Dopamine has profound effects on behavior as highlighted in previous studies (13-16). Nevertheless, the contribution of dopamine D1 receptor (D1R) in assessing reward information at neural level and its link to behaviors such as spatial associative learning remains to be specified. In the present study, we used knockout mice lacking D1R (D1R-KO) and their wild-type (WT) littermates to examine the contribution of this receptor in mediating reward, locomotion, and spatial learning and in regulating neural responses to prediction of reward. These mice were tested for their ability to perform several spatial tasks, including random reward place search task (RRPST) and place learning task (PLT), by using intracranial self-stimulation (ICSS) as rewards (15). To investigate the involvement of D1R functions in reward processing and spatial associative processes, we recorded neural activity from the NAc of D1R-KO mice and their WT litte...

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Contribution of hippocampal place cell activity to learning and formation of goal-directed navigation in rats

Cited by 64 publications

References 60 publications

Goal-Related Activity in Hippocampal Place Cells

Goal-Related Activity in Hippocampal Place Cells

Topography of Arc/Arg3.1 mRNA Expression in the Dorsal and Ventral Hippocampus Induced by Recent and Remote Spatial Memory Recall: Dissociation of CA3 and CA1 Activation

Dopamine D1 receptors involved in locomotor activity and accumbens neural responses to prediction of reward associated with place

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