Maturational dynamics of hippocampal place cells in immature rats

Abstract

The ontogeny of neural substrates underlying episodic memory is not well described. Place cells are a surrogate for episodic memory and are important for spatial navigation in rodents. Although place cells are well described in mature brains, the nature of the maturation processes remains uncertain. We now report on the ontogeny of the place cell system in rats between P22 and P43, a time during which there is rapid improvement in spatial behavior. We found that place cells with adult like firing fields were observed at the earliest ages. However, at this age, adult like place cells were few in number and their place fields were not stable across multiple exposures to the same environment. Finally, independently of confounding factors such as the number of exposures to the environment, the proportion of adult-like place cells, their firing rate and their stability increased with age and the average spatial signal of all pyramidal cells improved. This finding could account for the poor spatial behavior observed at young ages (P20-P30) and suggests that a small number of adult-like place cells are insufficient to support navigation.The notion that hippocampus plays a critical role in the formation and storage of spatial memory is supported by the existence in rats (O'Keefe and Dostrovsky, 1971) and humans (Ekstrom et al., 2003) of neurons called place cells that encode the spatial location of the individual in the environment (Nadel, 1991;Rolls and Xiang, 2006). The place cell system has been suggested as a surrogate for episodic memory in humans (Eichenbaum et al., 1999) and place cell discharge properties provide useful access to the integrity of the networks supporting episodic memory. For instance, the signal quality of place cells (spatial coherence; (Kubie et al., 1990)) and the information content of their firing (Skaggs et al., 1993) provide information on the computational properties of these networks. In addition, place field stability across multiple exposures to the environment reflects the ability of these networks to consolidate information in memory. Currently it remains uncertain whether maturational processes are required for the establishment of a mature place cell network and if the timeframe of this maturation correlates with the already known development of spatial cognition. Establishing normal ontogeny of place cells is important as it may shed light on the phenomenon of infantile amnesia (Ruffman et al., 2001). In addition, neurological disease may impact developmental processes with long term adverse consequences and in Correspondence to: Rod C Scott, Department of Neurology, Neuroscience Center at Dartmouth, Dartmouth Medical School, One Medical Center Drive, Lebanon, New Hampshire 03756, Telephone: 603-650-4211, rscott@ich.ucl.ac.uk. Author ContributionsAll authors designed and carried out the experiments. R.C.S and P-P.L.S carried out the data collection and carried out the analyses. All authors wrote and approved the manuscript. NIH Public Access Author ManuscriptHippocampus. A...

Developmental studies of the hippocampus and hippocampal-dependent behaviors: Insights from interdisciplinary studies and tips for new investigators

“…However, age-related increases in the number of place cells, spatial coherence and inter-trial stability were noted beyond the end of the third postnatal week, along with increases in theta power measured from LFPs and entorhinal grid stability. Many of these developmental changes were corroborated in a later study highlighting an increase in the proportion of adult-like place cells, average spatial signal, and place field stability from P23 to P35 (Scott et al, 2011). No studies have yet correlated developmental alterations in spatial behavior with place or grid cell metrics or the concomitant increase in theta power (Hasselmo, 2005; Vanderwolf, 1969).…”

Ontogeny of contextual fear memory formation, specificity, and persistence in mice

“…Specifically, the developmental onset of contextual fear learning coincides with the onset of training-induced hippocampal immediate early gene expression (Raineki et al 2010), and lesion or inactivation of the hippocampus blocks the formation of context and contextual fear memories in infant rats (Foster and Burman 2010;Raineki et al 2010;Schiffino et al 2011). Therefore, the emerging ability of mice to form context-shock associations at 13-14 d of age may reflect the functional maturation of the hippocampus, which continues to undergo changes in neuron number (Altman and Bayer 1975), dendritic arborization (Rahimi and Claiborne 2007), signaling mechanisms (Paylor et al 1996), synaptic plasticity (Harris and Teyler 1984), and spatial firing (Langston et al 2010;Wills et al 2010;Scott et al 2011) during the postnatal period.…”

Attractor Dynamics of Spatially Correlated Neural Activity in the Limbic System

“…Some have suggested that the weights can be learned through a developmental process in which topographically organized representations are initially present to serve as a teacher to the attractor and then disappear (McNaughton et al 2006). The feasibility of these ideas may be tested in experiments that measure the developmental onset of place, grid, and directional signals (Martin & Berthoz 2002, Langston et al 2010, Wills et al 2010, Scott et al 2011). However, there is as yet no consensus theory or model of self-organization of weights of an attractor map, and such a model would help guide interpretation and analysis of the experimental results.…”