Abstract

This article describes a neural model of the anatomy, neurophysiology, and functions of intrinsic and extrinsic theta rhythms in the brains of multiple species. Topics include how theta rhythms were discovered; how theta rhythms organize brain information processing into temporal series of spatial patterns; how distinct theta rhythms occur within area CA1 of the hippocampus and between the septum and area CA3 of the hippocampus; what functions theta rhythms carry out in different brain regions, notably CA1-supported functions like learning, recognition, and memory that involve visual, cognitive, and emotional processes; how spatial navigation, adaptively timed learning, and category learning interact with hippocampal theta rhythms; how parallel cortical streams through the lateral entorhinal cortex (LEC) and the medial entorhinal cortex (MEC) represent the end-points of the What cortical stream for perception and cognition and the Where cortical stream for spatial representation and action; how the neuromodulator acetylcholine interacts with the septo-hippocampal theta rhythm and modulates category learning; what functions are carried out by other brain rhythms, such as gamma and beta oscillations; and how gamma and beta oscillations interact with theta rhythms. Multiple experimental facts about theta rhythms are unified and functionally explained by this theoretical synthesis.

Highlights

  • A Neural Model of Intrinsic and Extrinsic Hippocampal Theta RhythmsMarcelo Mattar, University of California, San Diego, United States Homero Esmeraldo, University of California, San Diego, United States, in collaboration with reviewer MM

  • Spatial representations in the dorsal, or Where, cortical stream for spatial representation and action go through postrhinal cortex and medial entorhinal cortex (MEC) on their way to hippocampal cortex, whereas object representations in the ventral, or What, cortical stream for perception and object recognition go through perirhinal cortex and lateral entorhinal cortex (LEC) on their way to hippocampal cortex (Hargreaves et al, 2005; Norman and Eacott, 2005; Aminoff et al, 2007; Kerr et al, 2007; Eichenbaum and Lipton, 2008; van Strien et al, 2009; LaChance et al, 2019; Nilssen et al, 2019; Sethumadhavan et al, 2020), where they are merged

  • These parallel and homologous spatial and temporal representations may clarify the role of hippocampus in supporting episodic learning and memory (Tulving, 1972; Tulving and Thomson, 1973), since each episode in memory consists of specific spatio-temporal combinations of cues, imagery, and behaviors

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Summary

A Neural Model of Intrinsic and Extrinsic Hippocampal Theta Rhythms

Marcelo Mattar, University of California, San Diego, United States Homero Esmeraldo, University of California, San Diego, United States, in collaboration with reviewer MM. This article describes a neural model of the anatomy, neurophysiology, and functions of intrinsic and extrinsic theta rhythms in the brains of multiple species. Multiple experimental facts about theta rhythms are unified and functionally explained by this theoretical synthesis.

INTRODUCTION
Hippocampal Place Cells
Entorhinal Grid Cells
Stripe Cells
Temporal-to-Spatial
Episodic Learning and Memory
Linking Theta Rhythm to Grid Cells and Place Cells
Behaviors During Which Theta Rhythm Occurs
Intrinsic Theta Rhythm and Cholinergically Modulated Extrinsic Theta Rhythm
How Reduction of Cholinergic Input to Grid Cells Causes Their Collapse
Breakdowns in Vigilance Control of ART Dynamics Clarifies Mental Disorders
Gamma and Beta Oscillations Covary With PN and N200 Event-Related Potentials
What Happens to Place Cells When Grid Cells Collapse?
Disinhibition of the Septal Theta Rhythm via the Basal Ganglia
3.10. Toward Comprehensive Neural Architectures
INTRINSIC THETA RHYTHM DISSOCIATES LEARNED READ-OUT AND READ-IN
Competition Chooses Cells That Trigger Back-Propagating Teaching Signals
Gated Dipole Fields
Why Phase Precession of the Theta Rhythm?
Theta-Modulated Gamma Rhythms
ADAPTIVELY TIMED REGULATION OF CATEGORY LEARNING
CONCLUDING REMARKS
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