Close but no cigar: Spatial precision deficits following medial temporal lobe lesions provide novel insight into theoretical models of navigation and memory

Branden S. Kolarik, Trevor Baer, Kiarash Shahlaie, Andrew P. Yonelinas, Arne D. Ekstrom

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Increasing evidence suggests that the human hippocampus contributes to a range of different behaviors, including episodic memory, language, short-term memory, and navigation. A novel theoretical framework, the Precision and Binding Model, accounts for these phenomenon by describing a role for the hippocampus in high-resolution, complex binding. Other theories like Cognitive Map Theory, in contrast, predict a specific role for the hippocampus in allocentric navigation, while Declarative Memory Theory predicts a specific role in delay-dependent conscious memory. Navigation provides a unique venue for testing these predictions, with past results from research with humans providing inconsistent findings regarding the role of the human hippocampus in spatial navigation. Here, we tested five patients with lesions primarily restricted to the hippocampus and those extending out into the surrounding medial temporal lobe cortex on a virtual water maze task. Consistent with the Precision and Binding Model, we found partially intact allocentric memory in all patients, with impairments in the spatial precision of their searches for a hidden target. We found similar impairments at both immediate and delayed testing. Our findings are consistent with the Precision and Binding Model of hippocampal function, arguing for its role across domains in high-resolution, complex binding. Significance Statement: Remembering goal locations in one's environment is a critical skill for survival. How this information is represented in the brain is still not fully understood, but is believed to rely in some capacity on structures in the medial temporal lobe. Contradictory findings from studies of both humans and animals have been difficult to reconcile with regard to the role of the MTL, specifically the hippocampus. By assessing impairments observed during navigation to a goal in patients with medial temporal lobe damage we can better understand the role these structures play in such behavior. Utilizing virtual reality and novel analysis techniques, we have more precisely assessed the impact that medial temporal lobe damage has on spatial memory and navigation.

Original languageEnglish (US)
Pages (from-to)31-41
Number of pages11
JournalHippocampus
Volume28
Issue number1
DOIs
StatePublished - Jan 1 2018

Fingerprint

Temporal Lobe
Tobacco Products
Hippocampus
Theoretical Models
Episodic Memory
Short-Term Memory
Language
Survival
Water
Brain
Research

Keywords

  • Hippocampus
  • Lesions
  • Medial Temporal Lobe
  • Spatial Navigation

ASJC Scopus subject areas

  • Cognitive Neuroscience

Cite this

Close but no cigar : Spatial precision deficits following medial temporal lobe lesions provide novel insight into theoretical models of navigation and memory. / Kolarik, Branden S.; Baer, Trevor; Shahlaie, Kiarash; Yonelinas, Andrew P.; Ekstrom, Arne D.

In: Hippocampus, Vol. 28, No. 1, 01.01.2018, p. 31-41.

Research output: Contribution to journalArticle

@article{e27f96b7c19b402aa9c58940d2e70719,
title = "Close but no cigar: Spatial precision deficits following medial temporal lobe lesions provide novel insight into theoretical models of navigation and memory",
abstract = "Increasing evidence suggests that the human hippocampus contributes to a range of different behaviors, including episodic memory, language, short-term memory, and navigation. A novel theoretical framework, the Precision and Binding Model, accounts for these phenomenon by describing a role for the hippocampus in high-resolution, complex binding. Other theories like Cognitive Map Theory, in contrast, predict a specific role for the hippocampus in allocentric navigation, while Declarative Memory Theory predicts a specific role in delay-dependent conscious memory. Navigation provides a unique venue for testing these predictions, with past results from research with humans providing inconsistent findings regarding the role of the human hippocampus in spatial navigation. Here, we tested five patients with lesions primarily restricted to the hippocampus and those extending out into the surrounding medial temporal lobe cortex on a virtual water maze task. Consistent with the Precision and Binding Model, we found partially intact allocentric memory in all patients, with impairments in the spatial precision of their searches for a hidden target. We found similar impairments at both immediate and delayed testing. Our findings are consistent with the Precision and Binding Model of hippocampal function, arguing for its role across domains in high-resolution, complex binding. Significance Statement: Remembering goal locations in one's environment is a critical skill for survival. How this information is represented in the brain is still not fully understood, but is believed to rely in some capacity on structures in the medial temporal lobe. Contradictory findings from studies of both humans and animals have been difficult to reconcile with regard to the role of the MTL, specifically the hippocampus. By assessing impairments observed during navigation to a goal in patients with medial temporal lobe damage we can better understand the role these structures play in such behavior. Utilizing virtual reality and novel analysis techniques, we have more precisely assessed the impact that medial temporal lobe damage has on spatial memory and navigation.",
keywords = "Hippocampus, Lesions, Medial Temporal Lobe, Spatial Navigation",
author = "Kolarik, {Branden S.} and Trevor Baer and Kiarash Shahlaie and Yonelinas, {Andrew P.} and Ekstrom, {Arne D.}",
year = "2018",
month = "1",
day = "1",
doi = "10.1002/hipo.22801",
language = "English (US)",
volume = "28",
pages = "31--41",
journal = "Hippocampus",
issn = "1050-9631",
publisher = "Wiley-Liss Inc.",
number = "1",

}

TY - JOUR

T1 - Close but no cigar

T2 - Spatial precision deficits following medial temporal lobe lesions provide novel insight into theoretical models of navigation and memory

AU - Kolarik, Branden S.

AU - Baer, Trevor

AU - Shahlaie, Kiarash

AU - Yonelinas, Andrew P.

AU - Ekstrom, Arne D.

PY - 2018/1/1

Y1 - 2018/1/1

N2 - Increasing evidence suggests that the human hippocampus contributes to a range of different behaviors, including episodic memory, language, short-term memory, and navigation. A novel theoretical framework, the Precision and Binding Model, accounts for these phenomenon by describing a role for the hippocampus in high-resolution, complex binding. Other theories like Cognitive Map Theory, in contrast, predict a specific role for the hippocampus in allocentric navigation, while Declarative Memory Theory predicts a specific role in delay-dependent conscious memory. Navigation provides a unique venue for testing these predictions, with past results from research with humans providing inconsistent findings regarding the role of the human hippocampus in spatial navigation. Here, we tested five patients with lesions primarily restricted to the hippocampus and those extending out into the surrounding medial temporal lobe cortex on a virtual water maze task. Consistent with the Precision and Binding Model, we found partially intact allocentric memory in all patients, with impairments in the spatial precision of their searches for a hidden target. We found similar impairments at both immediate and delayed testing. Our findings are consistent with the Precision and Binding Model of hippocampal function, arguing for its role across domains in high-resolution, complex binding. Significance Statement: Remembering goal locations in one's environment is a critical skill for survival. How this information is represented in the brain is still not fully understood, but is believed to rely in some capacity on structures in the medial temporal lobe. Contradictory findings from studies of both humans and animals have been difficult to reconcile with regard to the role of the MTL, specifically the hippocampus. By assessing impairments observed during navigation to a goal in patients with medial temporal lobe damage we can better understand the role these structures play in such behavior. Utilizing virtual reality and novel analysis techniques, we have more precisely assessed the impact that medial temporal lobe damage has on spatial memory and navigation.

AB - Increasing evidence suggests that the human hippocampus contributes to a range of different behaviors, including episodic memory, language, short-term memory, and navigation. A novel theoretical framework, the Precision and Binding Model, accounts for these phenomenon by describing a role for the hippocampus in high-resolution, complex binding. Other theories like Cognitive Map Theory, in contrast, predict a specific role for the hippocampus in allocentric navigation, while Declarative Memory Theory predicts a specific role in delay-dependent conscious memory. Navigation provides a unique venue for testing these predictions, with past results from research with humans providing inconsistent findings regarding the role of the human hippocampus in spatial navigation. Here, we tested five patients with lesions primarily restricted to the hippocampus and those extending out into the surrounding medial temporal lobe cortex on a virtual water maze task. Consistent with the Precision and Binding Model, we found partially intact allocentric memory in all patients, with impairments in the spatial precision of their searches for a hidden target. We found similar impairments at both immediate and delayed testing. Our findings are consistent with the Precision and Binding Model of hippocampal function, arguing for its role across domains in high-resolution, complex binding. Significance Statement: Remembering goal locations in one's environment is a critical skill for survival. How this information is represented in the brain is still not fully understood, but is believed to rely in some capacity on structures in the medial temporal lobe. Contradictory findings from studies of both humans and animals have been difficult to reconcile with regard to the role of the MTL, specifically the hippocampus. By assessing impairments observed during navigation to a goal in patients with medial temporal lobe damage we can better understand the role these structures play in such behavior. Utilizing virtual reality and novel analysis techniques, we have more precisely assessed the impact that medial temporal lobe damage has on spatial memory and navigation.

KW - Hippocampus

KW - Lesions

KW - Medial Temporal Lobe

KW - Spatial Navigation

UR - http://www.scopus.com/inward/record.url?scp=85038581330&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85038581330&partnerID=8YFLogxK

U2 - 10.1002/hipo.22801

DO - 10.1002/hipo.22801

M3 - Article

C2 - 28888032

AN - SCOPUS:85038581330

VL - 28

SP - 31

EP - 41

JO - Hippocampus

JF - Hippocampus

SN - 1050-9631

IS - 1

ER -