In vitro characterization of gamma oscillations in the hippocampal formation of the domestic chick

Abstract

Avian and mammalian brains have evolved independently from each other for about 300 million years. During that time, the hippocampal formation (HF) has diverged in morphology and cytoarchitecture, but seems to have conserved much of its function. It is therefore an open question how seemingly different neural organizations can generate the same function. A prominent feature of the mammalian hippocampus is that it generates different neural oscillations, including the gamma rhythm, which plays an important role in memory processing. In this study, we investigate whether the avian hippocampus also generates gamma oscillations, and whether similar pharmacological mechanisms are involved in this function. We investigated the existence of gamma oscillations in avian HF using in vitro electrophysiology in P0-P12 domestic chick (Gallus gallus domesticus) HF brain slices. Persistent gamma frequency oscillations were induced by the bath application of the cholinergic agonist carbachol, but not by kainate, a glutamate receptor agonist. Similar to other species, carbachol-evoked gamma oscillations were sensitive to GABA_A , AMPA/kainate and muscarinic (M1) receptor antagonism. Therefore, similar to mammalian species, muscarinic receptor-activated avian HF gamma oscillations may arise via a pyramidal-interneuron gamma (PING)-based mechanism. Gamma oscillations are most prominent in the ventromedial area of the hippocampal slices, and gamma power is reduced more laterally and dorsally in the HF. We conclude that similar micro-circuitry may exist in the avian and mammalian hippocampal formation, and this is likely to relate to the shared function of the two structures.

Keywords: Gallus gallus domesticus; avian hippocampus; homology; local field potentials; rhythmogenesis.

Figure 1

(A) Example induction of gamma oscillations using different concentrations of carbachol in the same slice. (B) Spectrograms of gamma oscillations. Different colours represent different concentrations of carbachol: black: 0 μm; orange: 1 μm; green: 2 μm; purple: 5 μm; red: 10 μm. (C) Carbachol significantly increases the power (area under the curve) in the gamma band in a dose‐dependent measure. There is a significant induction of gamma oscillations with 1 μm of carbachol and a significant increase in power with 2 μm. The increase from 2 to 10 μm is not statistically significant due to high variability among slices, as indicated by the grey lines, which each represent a different slice.

Figure 2

(A) Change in area under the curve gamma power after treatment with the different pharmacological agents, expressed as a percentage of the gamma power before adding the drug. Individual points represent separate slices, while the bars represent means + SEM. (B) Change in peak frequency after treatment with the different pharmacological agents. Atr = 1 μm Atropine; Scop = 10 μm Scopolamine; Pir = 1 μm Pirenzepine; Gabaz = 1 μm Gabazine; NBQX = 20 μm NBQX; D‐AP5 = 50 μm D‐AP5. *P < 0.05; **P < 0.01; ***P < 0.001. Connected points represent the change within one slice. Bars represent means + SEM.

Figure 3

(A) Example of distribution of gamma power around an anterior coronal hippocampal slice from the chicken brain (image from Brainmaps.org). The inset shows parvalbumin‐positive cells in the chick hippocampal formation. VT, ventral tip; VM, ventromedial; VL, ventrolateral; MM, middle medial; ML, middle lateral; DM, dorsomedial; DL, dorsolateral. (B) Area under the curve gamma power, normalized to the power in the ventromedial region. Power is lower as the electrode is moved both from medial to lateral and from ventral to dorsal. Ventral tip was left out of this analysis (see text). Individual points represent separate slices. Although the analysis was performed as a repeated‐measures analysis, the points derived from the same slices have not been connected with each other to keep the graph simple.