Developmental Changes in Hippocampal CA1 Single Neuron Firing and Theta Activity during Associative Learning.

Jangjin Kim,Mary E Goldsberry,John H Freeman,Thomas C Harmon,Fred J Helmstetter

doi:10.1371/journal.pone.0164781

Abstract

Hippocampal development is thought to play a crucial role in the emergence of many forms of learning and memory, but ontogenetic changes in hippocampal activity during learning have not been examined thoroughly. We examined the ontogeny of hippocampal function by recording theta and single neuron activity from the dorsal hippocampal CA1 area while rat pups were trained in associative learning. Three different age groups [postnatal days (P)17-19, P21-23, and P24-26] were trained over six sessions using a tone conditioned stimulus (CS) and a periorbital stimulation unconditioned stimulus (US). Learning increased as a function of age, with the P21-23 and P24-26 groups learning faster than the P17-19 group. Age- and learning-related changes in both theta and single neuron activity were observed. CA1 pyramidal cells in the older age groups showed greater task-related activity than the P17-19 group during CS-US paired sessions. The proportion of trials with a significant theta (4–10 Hz) power change, the theta/delta ratio, and theta peak frequency also increased in an age-dependent manner. Finally, spike/theta phase-locking during the CS showed an age-related increase. The findings indicate substantial developmental changes in dorsal hippocampal function that may play a role in the ontogeny of learning and memory.

Highlights

Hippocampal maturation has been proposed to be an important factor in the ontogeny of learning and memory [1]
The current study further examined the development of hippocampal modulation of eyeblink conditioning by examining theta and single-neuron activity in the dorsal hippocampal CA1 region while rat pups were trained in eyeblink conditioning on P17-19, P21-23, and P24-26
Greater task-related CA1 pyramidal cell activity was found in the older age groups (P21-23 and P24-26) relative to the youngest age group (P17-19)

Summary

Introduction

Hippocampal maturation has been proposed to be an important factor in the ontogeny of learning and memory [1]. Most of the evidence for the hippocampal maturation hypothesis comes from behavioral and lesion studies showing developmental changes in acquisition and retention of hippocampus-dependent tasks [2,3]. Rodent studies have found that spatial delayed alternation and hidden platform localization in the water maze become robust around the third postnatal week [4,5,6]. Context conditioning and the context pre-exposure facilitation effect develop around the third postnatal week in rats [2,7,8,9,10]. The ontogenetic emergence of these tasks and others suggest that the efficacy of hippocampal contributions to learning increases between postnatal day (P) 17 and 24 in rats.

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Results

Conclusion