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The Hippocampus and Dorsolateral Striatum Integrate Distinct Types of Memories through Time and Space, Respectively.
J Neurosci. 2020 11 18; 40(47):9055-9065.JN

Abstract

Several decades of research have established that different kinds of memories result from the activity of discrete neural networks. Studying how these networks process information in experiments that target specific types of mnemonic representations has provided deep insights into memory architecture and its neural underpinnings. However, in natural settings reality confronts organisms with problems that are not neatly compartmentalized. Thus, a critical problem in memory research that still needs to be addressed is how distinct types of memories are ultimately integrated. Here we demonstrate how two memory networks, the hippocampus and dorsolateral striatum, may accomplish such a goal. The hippocampus supports memory for facts and events, collectively known as declarative memory and often studied as spatial memory in rodents. The dorsolateral striatum provides the basis for habits that are assessed in stimulus-response types of tasks. Expanding previous findings, the current work revealed that in male Long-Evans rats, the hippocampus and dorsolateral striatum use time and space in distinct and largely complementary ways to integrate spatial and habitual representations. Specifically, the hippocampus supported both types of memories when they were formed in temporal juxtaposition, even if the learning took place in different environments. In contrast, the lateral striatum supported both types of memories if they were formed in the same environment, even at temporally distinct points. These results reveal for the first time that by using fundamental aspects of experience in specific ways, the hippocampus and dorsolateral striatum can transcend their attributed roles in information storage.SIGNIFICANCE STATEMENT The current paradigm in memory research postulates that different types of memories reflected in separate types of behavioral strategies result from activity in distinct neural circuits. However, recent data have shown that when rats concurrently acquired in the same environment of hippocampal-dependent spatial navigation and striatal-dependent approach of a visual cue, each of the two types of memories became dependent on both the hippocampus and dorsolateral striatum. The current work reveals that the hippocampus and dorsolateral striatum use distinct and complementary principles to integrate different types of memories in time and space: the hippocampus integrates memories formed in temporal proximity, while the lateral striatum integrates memories formed in the same space.

Authors+Show Affiliations

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

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural

Language

eng

PubMed ID

33051349

Citation

Ferbinteanu, Janina. "The Hippocampus and Dorsolateral Striatum Integrate Distinct Types of Memories Through Time and Space, Respectively." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 40, no. 47, 2020, pp. 9055-9065.
Ferbinteanu J. The Hippocampus and Dorsolateral Striatum Integrate Distinct Types of Memories through Time and Space, Respectively. J Neurosci. 2020;40(47):9055-9065.
Ferbinteanu, J. (2020). The Hippocampus and Dorsolateral Striatum Integrate Distinct Types of Memories through Time and Space, Respectively. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 40(47), 9055-9065. https://doi.org/10.1523/JNEUROSCI.1084-20.2020
Ferbinteanu J. The Hippocampus and Dorsolateral Striatum Integrate Distinct Types of Memories Through Time and Space, Respectively. J Neurosci. 2020 11 18;40(47):9055-9065. PubMed PMID: 33051349.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The Hippocampus and Dorsolateral Striatum Integrate Distinct Types of Memories through Time and Space, Respectively. A1 - Ferbinteanu,Janina, Y1 - 2020/10/13/ PY - 2020/05/06/received PY - 2020/09/04/revised PY - 2020/09/18/accepted PY - 2020/10/15/pubmed PY - 2021/2/17/medline PY - 2020/10/14/entrez KW - cognitive memory KW - functional principles of memory circuits KW - habits KW - hippocampus KW - memory integration KW - memory systems KW - striatum SP - 9055 EP - 9065 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J Neurosci VL - 40 IS - 47 N2 - Several decades of research have established that different kinds of memories result from the activity of discrete neural networks. Studying how these networks process information in experiments that target specific types of mnemonic representations has provided deep insights into memory architecture and its neural underpinnings. However, in natural settings reality confronts organisms with problems that are not neatly compartmentalized. Thus, a critical problem in memory research that still needs to be addressed is how distinct types of memories are ultimately integrated. Here we demonstrate how two memory networks, the hippocampus and dorsolateral striatum, may accomplish such a goal. The hippocampus supports memory for facts and events, collectively known as declarative memory and often studied as spatial memory in rodents. The dorsolateral striatum provides the basis for habits that are assessed in stimulus-response types of tasks. Expanding previous findings, the current work revealed that in male Long-Evans rats, the hippocampus and dorsolateral striatum use time and space in distinct and largely complementary ways to integrate spatial and habitual representations. Specifically, the hippocampus supported both types of memories when they were formed in temporal juxtaposition, even if the learning took place in different environments. In contrast, the lateral striatum supported both types of memories if they were formed in the same environment, even at temporally distinct points. These results reveal for the first time that by using fundamental aspects of experience in specific ways, the hippocampus and dorsolateral striatum can transcend their attributed roles in information storage.SIGNIFICANCE STATEMENT The current paradigm in memory research postulates that different types of memories reflected in separate types of behavioral strategies result from activity in distinct neural circuits. However, recent data have shown that when rats concurrently acquired in the same environment of hippocampal-dependent spatial navigation and striatal-dependent approach of a visual cue, each of the two types of memories became dependent on both the hippocampus and dorsolateral striatum. The current work reveals that the hippocampus and dorsolateral striatum use distinct and complementary principles to integrate different types of memories in time and space: the hippocampus integrates memories formed in temporal proximity, while the lateral striatum integrates memories formed in the same space. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/33051349/The_Hippocampus_and_Dorsolateral_Striatum_Integrate_Distinct_Types_of_Memories_through_Time_and_Space_Respectively_ L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=33051349 DB - PRIME DP - Unbound Medicine ER -