Abstract

Previous neurophysiological and behavioral studies relate hippocampal functions to place learning and memory, and encoding of task (or context)-specific information. Encoding of both task-specific information and own location is essential for episodic memory and for animals to navigate to reward-related places. It is suggested that different neural circuits with different assemblies of different hippocampal neurons are created in different environments or behavioral contexts for the hippocampal formation (HF) to encode and retrieve episodic memory. To investigate whether synchronous activity of hippocampal neurons, suggesting functional connectivity between those neurons, is task and position dependent, multiple single unit activities were recorded during performance of real and virtual translocation (VT) tasks. The monkey moved to one of four reward areas by driving a cab (real translocation) or by moving a pointer on a monitor. Of 163 neuron pairs, significant peaks in cross-correlograms (CCGs) were observed in 98 pairs. Most CCGs had positive peaks within 50 ms. Task-dependent cross-correlations (CCRs) were observed in 44% of the neuron pairs, and similarly observed in both the real and VT tasks. These CCRs were frequently observed in pyramidal vs. pyramidal neuron pairs with positive peak and peak shift. However, no consistent patterns of peak polarity, peak shift, and neuronal types were seen in task-independent CCRs. There was no significant difference in frequency of CCG peaks between real and VT tasks. These results suggest that the task-dependent information may be encoded by interaction among pyramidal neurons, and the common information across tasks may be encoded by interaction among pyramidal neurons and interneurons in the HF. These neuronal populations could provide a neural basis for episodic memory to disambiguously guide animals to places associated with reward in different situations.

Highlights

  • It has been suggested that food-storing birds use memory to retrieve stored food and have a larger hippocampal formation (HF; Clayton, 1995)

  • To understand the relationship between spatial selectivity and taskdependency of HF neurons, we have investigated the neuronal activities in allocentric space in real and virtual translocation (VT), in which the monkey in a movable cab could freely move toward a destination by manipulating a joystick (Ono et al, 1993; Nishijo et al, 1997; Matsumura et al, 1999; Hori et al, 2003)

  • These data indicate that pyramidal vs. pyramidal neuron pairs with positive CCG peaks and peak shift contribute to both task-dependent and independent information processing, and that neuron pairs both with and without peak shift contribute to taskindependent information processing. These results suggest some important characteristics of functional connectivity in the HF that pyramidal neuron vs. pyramidal neuron pairs with positive peak and peak shift www.frontiersin.org

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Summary

Introduction

It has been suggested that food-storing birds use memory to retrieve stored food and have a larger hippocampal formation (HF; Clayton, 1995). The HF is involved in conditioned place preference in which animals learned to prefer a chamber where a conditioned stimulus was associated with sucrose solution (Ito et al, 2006, 2008) These results suggest that the HF is important in mapping the location of rewards, and in guiding animals to places previously associated with reward. Recent neuropsychological studies in humans have demonstrated a pivotal role of the medial temporal lobe including the HF and PH and its related areas in allocentric spatial information processing (Maguire et al, 1996a; Abrahams et al, 1997; Takahashi et al, 1997). Consistent with these studies, positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) have revealed blood flow increase in the HF and PH during various types of spatial tasks using a real or realistic virtual environment in normal humans (Aguirre et al, 1996; Ghaem et al, 1997; Maguire et al, 1997; Mellet et al, 2000)

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