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Contributions of Hippocampus and Striatum to Memory-Guided Behavior Depend on Past Experience.
J Neurosci. 2016 06 15; 36(24):6459-70.JN

Abstract

The hippocampal and striatal memory systems are thought to operate independently and in parallel in supporting cognitive memory and habits, respectively. Much of the evidence for this principle comes from double dissociation data, in which damage to brain structure A causes deficits in Task 1 but not Task 2, whereas damage to structure B produces the reverse pattern of effects. Typically, animals are explicitly trained in one task. Here, we investigated whether this principle continues to hold when animals concurrently learn two types of tasks. Rats were trained on a plus maze in either a spatial navigation or a cue-response task (sequential training), whereas a third set of rats acquired both (concurrent training). Subsequently, the rats underwent either sham surgery or neurotoxic lesions of the hippocampus (HPC), medial dorsal striatum (DSM), or lateral dorsal striatum (DSL), followed by retention testing. Finally, rats in the sequential training condition also acquired the novel "other" task. When rats learned one task, HPC and DSL selectively supported spatial navigation and cue response, respectively. However, when rats learned both tasks, HPC and DSL additionally supported the behavior incongruent with the processing style of the corresponding memory system. Thus, in certain conditions, the hippocampal and striatal memory systems can operate cooperatively and in synergism. DSM significantly contributed to performance regardless of task or training procedure. Experience with the cue-response task facilitated subsequent spatial learning, whereas experience with spatial navigation delayed both concurrent and subsequent response learning. These findings suggest that there are multiple operational principles that govern memory networks.

SIGNIFICANCE STATEMENT

Currently, we distinguish among several types of memories, each supported by a distinct neural circuit. The memory systems are thought to operate independently and in parallel. Here, we demonstrate that the hippocampus and the dorsal striatum memory systems operate independently and in parallel when rats learn one type of task at a time, but interact cooperatively and in synergism when rats concurrently learn two types of tasks. Furthermore, new learning is modulated by past experiences. These results can be explained by a model in which independent and parallel information processing that occurs in the separate memory-related neural circuits is supplemented by information transfer between the memory systems at the level of the cortex.

Authors+Show Affiliations

Departments of Physiology and Pharmacology and Neurology, State University of New York Downstate Medical Center, Brooklyn, New York 11203 janina.ferbinteanu@downstate.edu ferbinteanu@gmail.com.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

27307234

Citation

Ferbinteanu, Janina. "Contributions of Hippocampus and Striatum to Memory-Guided Behavior Depend On Past Experience." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 36, no. 24, 2016, pp. 6459-70.
Ferbinteanu J. Contributions of Hippocampus and Striatum to Memory-Guided Behavior Depend on Past Experience. J Neurosci. 2016;36(24):6459-70.
Ferbinteanu, J. (2016). Contributions of Hippocampus and Striatum to Memory-Guided Behavior Depend on Past Experience. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 36(24), 6459-70. https://doi.org/10.1523/JNEUROSCI.0840-16.2016
Ferbinteanu J. Contributions of Hippocampus and Striatum to Memory-Guided Behavior Depend On Past Experience. J Neurosci. 2016 06 15;36(24):6459-70. PubMed PMID: 27307234.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Contributions of Hippocampus and Striatum to Memory-Guided Behavior Depend on Past Experience. A1 - Ferbinteanu,Janina, PY - 2016/03/14/received PY - 2016/05/07/accepted PY - 2016/6/17/entrez PY - 2016/6/17/pubmed PY - 2017/7/14/medline KW - functional principles of memory circuits KW - hippocampus KW - learning KW - memory KW - memory systems KW - striatum SP - 6459 EP - 70 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J Neurosci VL - 36 IS - 24 N2 - UNLABELLED: The hippocampal and striatal memory systems are thought to operate independently and in parallel in supporting cognitive memory and habits, respectively. Much of the evidence for this principle comes from double dissociation data, in which damage to brain structure A causes deficits in Task 1 but not Task 2, whereas damage to structure B produces the reverse pattern of effects. Typically, animals are explicitly trained in one task. Here, we investigated whether this principle continues to hold when animals concurrently learn two types of tasks. Rats were trained on a plus maze in either a spatial navigation or a cue-response task (sequential training), whereas a third set of rats acquired both (concurrent training). Subsequently, the rats underwent either sham surgery or neurotoxic lesions of the hippocampus (HPC), medial dorsal striatum (DSM), or lateral dorsal striatum (DSL), followed by retention testing. Finally, rats in the sequential training condition also acquired the novel "other" task. When rats learned one task, HPC and DSL selectively supported spatial navigation and cue response, respectively. However, when rats learned both tasks, HPC and DSL additionally supported the behavior incongruent with the processing style of the corresponding memory system. Thus, in certain conditions, the hippocampal and striatal memory systems can operate cooperatively and in synergism. DSM significantly contributed to performance regardless of task or training procedure. Experience with the cue-response task facilitated subsequent spatial learning, whereas experience with spatial navigation delayed both concurrent and subsequent response learning. These findings suggest that there are multiple operational principles that govern memory networks. SIGNIFICANCE STATEMENT: Currently, we distinguish among several types of memories, each supported by a distinct neural circuit. The memory systems are thought to operate independently and in parallel. Here, we demonstrate that the hippocampus and the dorsal striatum memory systems operate independently and in parallel when rats learn one type of task at a time, but interact cooperatively and in synergism when rats concurrently learn two types of tasks. Furthermore, new learning is modulated by past experiences. These results can be explained by a model in which independent and parallel information processing that occurs in the separate memory-related neural circuits is supplemented by information transfer between the memory systems at the level of the cortex. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/27307234/Contributions_of_Hippocampus_and_Striatum_to_Memory_Guided_Behavior_Depend_on_Past_Experience_ L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=27307234 DB - PRIME DP - Unbound Medicine ER -