Deep layer neurons in the rat medial entorhinal cortex fire sparsely irrespective of spatial novelty

Abstract

Extracellular recordings in medial entorhinal cortex have revealed the existence of spatially-modulated firing patterns, which are thought to contribute to a cognitive map of external space. Previous work indicated that during exploration of novel environments, spiking activity in deep entorhinal layers is much sparser than in superficial layers. In the present report, we ask whether this laminar activity profile is a consequence of environmental novelty. We report on a large dataset of juxtacellularly-recorded neurons (n = 70) whose spiking activity was monitored while rats explored either a novel or a familiar environment, or both within the same session. Irrespective of previous knowledge of the environment, deep layer activity was very low during exploration (median firing rate 0.4 Hz for non-silent cells), with a large fraction of silent cells (n = 19 of a total 37), while superficial layer activity was several times higher (median firing rate 2.4 Hz; n = 33). The persistence of laminar differences in firing activity both under environmental novelty and familiarity, and even in head-restrained stationary animals, suggests that sparse coding might be a constitutive feature of deep entorhinal layers.

Keywords: medial entorhinal cortex; novelty; rat; sparse coding; spatial.

Figure 1

Deep layer neurons in MEC fire at low rates irrespective of spatial experience. (A) Top, reconstruction of the dendritic morphology of the L5 neuron of MEC recorded during exploration of a two-compartment maze (recording shown in D). Scale bar = 200 μm. Bottom, representative spike trace recorded during freely-moving behavior. (B) Firing locations of spikes (red) and trajectory of the rat (gray) during running in a novel environment (O-maze). Average firing rate is indicated. (C) Same as in (B), but for a familiar environment. (D) Top: The two-compartment maze used for the combined novel/familiar experiments. Bottom: as in (B), but for a recording in the two-compartment maze (square compartment, novel; rectangular compartment, familiar). Average firing rates in novel and familiar compartments are indicated. (E) Average firing rates of all juxtacellularly recorded neurons in novel and familiar environments. Horizontal lines connect recordings from the two-compartment maze, where novel and familiar compartments where sampled within the same recording session. Red lines indicate medians.

Figure 2

Superficial layer neurons in MEC fire at higher rates irrespective of spatial experience. (A) Top, reconstruction of the dendritic morphology of the L3 neuron of MEC recorded during exploration of a familiar O-maze [recording shown in (C)]. Bottom, representative spike trace. Scale bar = 200 during freely-moving behavior. (B) Firing locations of spikes (red) and trajectory of the rat (gray) during running in a novel environment (O- maze). Average firing rate is indicated. (C) Same as in (B), but for a familiar environment. (D) Top: the two-compartment maze used for the combined novel/familiar experiments. Bottom: as in (B), but for a recording in the two-compartment maze (square compartment, novel; rectangular compartment, familiar). Average firing rates in novel and familiar compartments are indicated. (E) Average firing rates of all juxtacellularly recorded neurons in novel and familiar environments. Horizontal lines connect recordings from the two-compartment maze, where novel and familiar compartments where sampled within the same recording session. Red lines indicate medians.

Figure 3

Layer is a strong determinant of average firing rate in MEC. (A) Cumulative distribution of average firing rates for all juxtacellularly recorded neurons recorded in novel (black, n = 57) and familiar environments (gray, n = 31). The two distributions are not statistically different [median for novel 0.54 (n = 57), familiar 0.17 (n = 31); p = 0.4, Wilcoxon rank-sum test]. (B) Cumulative distribution of average firing rates for all juxtacellularly recorded neurons recorded in superficial (light blue, n = 33) vs. deep layers (dark blue, n = 37), irrespective of spatial experience. The two distributions are statistically different (median for superficial 2.3, deep 0.0, p = 1.4 10⁻⁷, Wilcoxon rank-sum test).