Disconnection analysis of CA3 and DG in mediating encoding but not retrieval in a spatial maze learning task

Jerman, Taylor S.; Kesner, Raymond P.; Hunsaker, Michael R.

doi:10.1101/lm.246906

Cited by 67 publications

(81 citation statements)

References 26 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The assumption made in this analysis was that the encoding of spatial information predominated during day 1, and retrieval of consolidated spatial information predominated during the first five trials during day 2. The results from testing rats in the Hebb-Williams maze indicate that CA3a,b, but not CA1, lesions impair within-day learning (encoding) and CA1, but not CA3a,b, lesions impair retrieval across days (Jerman et al 2006;Vago et al 2007). Finally, CA3 lesioned rats are impaired in the standard water maze task, which requires multiple trials (Brun et al 2002;Florian and Roullet 2004), although mice that lacked NMDA receptors in CA3 do not appear to be impaired in learning the water maze (Nakazawa et al 2002).…”

Section: Encoding Over Multiple Trialsmentioning

confidence: 98%

Behavioral functions of the CA3 subregion of the hippocampus

2007

View full text Add to dashboard Cite

From a behavioral perspective, the CA3a,b subregion of the hippocampus plays an important role in the encoding of new spatial information within short-term memory with a duration of seconds and minutes. This can easily be observed in tasks that require rapid encoding, novelty detection, one-trial short-term or working memory, and one-trial cued recall primarily for spatial information. These are tasks that have been assumed to reflect the operations of episodic memory and require interactions between CA3a,b and the dentate gyrus via mossy fiber inputs into the CA3a,b. The CA3a,b is also important for encoding of spatial information requiring multiple trials including the acquisition of arbitrary and relational associations. These tasks tend to be non-episodic and can be mediated by arbitrary and conjunctive operations. All these tasks are assumed to operate within an autoassociative network function of the CA3 region. The output from CA3a,b via the fimbria and the medial and lateral perforant path inputs play a supporting role in the neural circuit that supports the operation of these tasks. The CA3a,b also plays a role in sequential processing of information in cooperation with CA1 based on the Schaffer collateral output from CA3a,b to CA1. The CA3a,b also supports retrieval of short-term memory information based on a spatial pattern completion process. Finally, CA3c may, in cooperation with the dentate gyrus, serve an important role in processing the geometry of the environment.This review article emphasizes the importance of behavioral functions of the CA3 subregion of the hippocampus. In the first section, I present a general overview of the anatomy of the hippocampus. In the second section, I present the influence of an autoassociative network function of the CA3 region in supporting mnemonic functions. In general terms, the data suggest that CA3a,b mediates the acquisition and encoding of spatial information within short-term memory with a duration of seconds and minutes. In the context of short-term memory, the CA3a,b mediates rapid encoding of especially spatial information, novelty detection, and one-trial cued recall (all forms of episodic memory). Also, CA3a,b mediates encoding of information requiring multiple trials to construct relational representations. It should be noted that CA3a,b can also be involved in short-term memory retrieval as evidenced by support for a pattern completion process. Finally, CA3c may contribute to pattern separation of the geometry of the environment. Spatial information represents the critical attribute or domain that is processed in CA3. In the third section, I emphasize that the mnemonic functions of the autoassociative network of CA3 depend on inputs into CA3 from other brain regions within the hippocampus (i.e., dentate gyrus) and brain regions outside the hippocampus (i.e., medial and lateral entorhinal cortex) as well as outputs from CA3 to brain regions within the hippocampus (i.e., dentate gyrus, CA1) and brain regions outside the hippocampus (i.e., medial and l...

show abstract

Section: Encoding Over Multiple Trialsmentioning

confidence: 98%

Behavioral functions of the CA3 subregion of the hippocampus

2007

View full text Add to dashboard Cite

show abstract

“…Given the observed selective deficits in retrieval of spatial cues necessary for navigation of a maze and previous evidence implicating CA1 in retrieval (Hasselmo, 1995;Hasselmo et al, 1995;Sybirska et al, 2000;Kesner et al, 2004;Lee and Kesner, 2004b;Jerman et al, 2006;Rolls and Kesner, 2006), we reasoned that similar selective deficits may be apparent in additional CA1-dependent tasks. It has been shown previously that CA3-lesioned rats are significantly impaired on the acquisition, but not retention of contextual fear-conditioning whereas, CA1 lesioned rats are significantly impaired on retention but not acquisition (Lee and Kesner, 2004a).…”

Section: The Effects Of Apomorphine On Acquisition Of Contextual Fearmentioning

confidence: 99%

“…Encoding of information acquired in a Hebb-Williams maze or in contextual fear conditioning, using a within-days analysis, is impaired by targeted lesions to the CA3 and dentate gyrus (DG) subregions, but not from targeted lesions to the CA1 subregion. In contrast, using a between-days analysis, retention and retrieval is disrupted following CA1, but not following CA3 or DG lesions (Lee and Kesner, 2004a;Lee and Kesner, 2004b;Jerman et al, 2006). Impairments have also been demonstrated in delay-dependent retrieval without impairing immediate recall or encoding of spatial information after infusing glutamatergic antagonists (Lee and Kesner, 2002), or cyclooxygenase-2 inhibitors (Sharifzadeh et al, 2006) into the CA1 subregion, but not when infused into the CA3 subregion.…”

Section: Introductionmentioning

confidence: 97%

“…The injection needle was left in place for 1 min after the injection to allow for proper diffusion. Previous research has shown that similar lesion methods have been well suited for selective lesions of CA subregions of the hippocampus Lee and Kesner, 2004a;Jerman et al, 2006). Following surgery, the rats were allowed to recover on a heating pad before returning to their home cage.…”

Section: Ca1 Lesionsmentioning

confidence: 99%

See 1 more Smart Citation

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

2007

Self Cite

View full text Add to dashboard Cite

Subregional analyses of the hippocampus have suggested a selective role for the CA1 subregion in intermediate/long-term spatial memory and consolidation, but not short-term acquisition or encoding processes. It remains unclear how the direct cortical projection to CA1 via the perforant path (pp) contributes to these CA1-dependent processes. It has been suggested that dopamine selectively modulates the pp projection to CA1 while having little to no effect on the Schaffer collateral (SC) projection to CA1. This series of behavioral and electro-physiological experiments takes advantage of this pharmacological dissociation to demonstrate that the direct pp inputs to CA1 are critical in CA1-dependent intermediate-term retention and retrieval function. Here we demonstrate that local infusion of the nonselective dopamine agonist, apomorphine (10, 15 μg), into the CA1 subregion of awake animals produces impairments in between-day retention and retrieval, sparing within-day encoding of a modified Hebb-Williams maze and contextual conditioning of fear. In contrast, apomorphine produces no deficits when infused into the CA3 subregion. To complement the behavioral analyses, electrophysiological data was collected. In anesthetized animals, local infusion of the same doses of apomorphine significantly modifies evoked responses in the distal dendrites of CA1 following angular bundle stimulation, but produces no significant effects in the more proximal dendritic layer following stimulation of the SC. These results support a modulatory role for dopamine in the EC-CA1, but not CA3-CA1 circuitry, and suggest the possibility of a more fundamental role for EC-CA1 synaptic transmission in terms of intermediate-term, but not short-term spatial memory.

show abstract

“…The CA1 region also appears to be involved in retrieval after longer time delays, with rats lesioned in the CA1 region having no difficulty in encoding new information but impaired in retrieval after a 24-h interval [100,212]. Additionally, lesions made in the CA1 region 24 h post training in a water maze disrupted subsequent recall, whilst CA1 lesions made 3 weeks later did not disrupt retrieval of task [164].…”

Section: Ca1 Region-role In Memory Retrievalmentioning

confidence: 99%

The impact of flavonoids on spatial memory in rodents: from behaviour to underlying hippocampal mechanisms

et al. 2009

View full text Add to dashboard Cite

Emerging evidence suggests that a group of dietary-derived phytochemicals known as flavonoids are able to induce improvements in memory, learning and cognition. Flavonoids have been shown to modulate critical neuronal signalling pathways involved in processes of memory, and therefore are likely to affect synaptic plasticity and long-term potentiation mechanisms, widely considered to provide a basis for memory. Animal dietary supplementation studies have further shown that flavonoidrich foods are able to reverse age-related spatial memory and spatial learning impairments. A more accurate understanding of how a particular spatial memory task works and of which aspects of memory and learning can be assessed in each case, are necessary for a correct interpretation of data relating to diet-cognition experiments. Further understanding of how specific behavioural tasks relate to the functioning of hippocampal circuitry during learning processes might be also elucidative of the specific observed memory improvements. The overall goal of this review is to give an overview of how the hippocampal circuitry operates as a memory system during behavioural tasks, which we believe will provide a new insight into the underlying mechanisms of the action of flavonoids on cognition.

show abstract

Disconnection analysis of CA3 and DG in mediating encoding but not retrieval in a spatial maze learning task

Cited by 67 publications

References 26 publications

Behavioral functions of the CA3 subregion of the hippocampus

Behavioral functions of the CA3 subregion of the hippocampus

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

The impact of flavonoids on spatial memory in rodents: from behaviour to underlying hippocampal mechanisms

Contact Info

Product

Resources

About