Abstract
The perirhinal cortex (PRC) is a polymodal associative region of the temporal lobe that works as a gateway between cortical areas and hippocampus. In recent years, an increasing interest arose in the role played by the PRC in learning and memory processes, such as object recognition memory, in contrast with certain forms of hippocampus-dependent spatial and episodic memory. The integrative properties of the PRC should provide all necessary resources to select and enhance the information to be propagated to and from the hippocampus. Among these properties, we explore in this paper the ability of the PRC neurons to amplify the output voltage to current input at selected frequencies, known as membrane resonance. Within cerebral circuits the resonance of a neuron operates as a filter toward inputs signals at certain frequencies to coordinate network activity in the brain by affecting the rate of neuronal firing and the precision of spike timing. Furthermore, the ability of the PRC neurons to resonate could have a fundamental role in generating subthreshold oscillations and in the selection of cortical inputs directed to the hippocampus. Here, performing whole-cell patch-clamp recordings from perirhinal pyramidal neurons and GABAergic interneurons of GAD67-GFP+ mice, we found, for the first time, that the majority of PRC neurons are resonant at their resting potential, with a resonance frequency of 0.5–1.5 Hz at 23°C and of 1.5–2.8 Hz at 36°C. In the presence of ZD7288 (blocker of HCN channels) resonance was abolished in both pyramidal neurons and interneurons, suggesting that Ih current is critically involved in resonance generation. Otherwise, application of TTx (voltage-dependent Na+ channel blocker) attenuates the resonance in pyramidal neurons but not in interneurons, suggesting that only in pyramidal neurons the persistent sodium current has an amplifying effect. These experimental results have also been confirmed by a computational model. From a functional point of view, the resonance in the PRC would affect the reverberating activity between neocortex and hippocampus, especially during slow wave sleep, and could be involved in the redistribution and strengthening of memory representation in cortical regions.
Highlights
The perirhinal cortex (PRC) is a polymodal associative ventral region of the temporal lobe located laterally to the rhinal sulcus
We found a more depolarized membrane resting potential in resonant compared to non-resonant neurons, FIGURE 4 | Relationships between firing patterns and resonant or non-resonant behavior of the PRC neurons. (A,B) Percentage of specific firing patterns for resonant (A) and non-resonant (B) PRC pyramidal neurons. (C) Percentage of resonant vs. non-resonant cells classified for a specific firing pattern of pyramidal neurons. (A –C ) Same as (A–C) for GABAergic interneurons
This paper describes for the first time the membrane resonance properties of pyramidal cells and GABAergic interneurons throughout the different layers of the mouse perirhinal cortex
Summary
The perirhinal cortex (PRC) is a polymodal associative ventral region of the temporal lobe located laterally to the rhinal sulcus. It is connected with many sensory and polymodal areas, reward-related cortices, and other structures of the medial temporal lobe (MTL) such as the entorhinal and postrhinal (or parahippocampal in primates) cortices, the amygdala (Pinto et al, 2006; Biella et al, 2010), and the hippocampus (Witter et al, 2000; Kealy and Commins, 2011; Suzuki and Naya, 2014). Based on cytoarchitectonic properties and anatomical connections, PRC should play a crucial role in processing information directed from and to the hippocampal formation. PRC importantly retains integrative properties that are essential for different memory and perceptual tasks (Biella et al, 2001; Murray and Richmond, 2001; Davachi, 2006; Staresina and Davachi, 2008; Suzuki and Naya, 2014)
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