Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex - PubMed (original) (raw)

Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex

Mario Galarreta et al. Proc Natl Acad Sci U S A. 2002.

Abstract

Networks of gamma-aminobutyric acid (GABA)ergic interneurons connected via electrical and chemical synapses are thought to play an important role in detecting and promoting synchronous activity in the cerebral cortex. Although the properties of electrical and chemical synaptic interactions among inhibitory interneurons are critical for their function as a network, they have only been studied systematically in juvenile animals. Here, we have used transgenic mice expressing the enhanced green fluorescent protein in cells containing parvalbumin (PV) to study the synaptic connectivity among fast-spiking (FS) cells in slices from adult animals (2-7 months old). We have recorded from pairs of PV-FS cells and found that the majority of them were electrically coupled (61%, 14 of 23 pairs). In addition, 78% of the pairs were connected via GABAergic chemical synapses, often reciprocally. The average coupling coefficient for step injections was 1.5% (n = 14), a smaller value than that reported in juvenile animals. GABA-mediated inhibitory postsynaptic currents and potentials decayed with exponential time constants of 2.6 and 5.9 ms, respectively, and exhibited paired-pulse depression (50-ms interval). The inhibitory synaptic responses in the adult were faster than those observed in young animals. Our results indicate that PV-FS cells are highly interconnected in the adult cerebral cortex by both electrical and chemical synapses, establishing networks that can have important implications for coordinating activity in cortical circuits.

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Figures

Fig 1.

Fig 1.

Identification of PV-expressing neurons in adult neocortical slices. (A) Fluorescing cells in a neocortical slice obtained from a 2-month-old PV-EGFP-expressing mouse. Three EGFP-expressing neurons are illustrated. (B) same field under differential interference contrast infrared videomicroscopy. Note the tip of the patch electrode used to record the activity of an EGFP-expressing neuron. (Scale bar, 10 μm.) (C) Firing pattern in response to current injection (190 pA, 300 ms) of the EGFP-expressing neuron illustrated in A and B (arrowhead). The three responses were obtained with the same current injection. Note the discharges of high-frequency nonaccommodating action potentials in the two upper traces.

Fig 2.

Fig 2.

(A) Neurolucida reconstruction of a pair of PV-FS cells simultaneously recorded in a slice from a 2-month-old mouse. The firing patterns of both cells in response to current injection (300 ms, 1 nA) are shown in the insets. (B) The injection of depolarizing (600-pA) or hyperpolarizing (150-pA) current in cell 1 simultaneously affected the membrane voltage of the noninjected cell 2. Step-coupling coefficient = 2.0%. Each trace is the average of 50 trials. Data are from the same pair illustrated in A. (C) Electrical coupling is bidirectional. Comparison of the step-coupling coefficient when current is injected in cell 1 versus cell 2 is shown.

Fig 3.

Fig 3.

Spike transmission through electrical synapses. (A) Spikelet obtained by subtracting supra- (1, thin traces) and subthreshold (2, thick traces) current injections in a pair of PV-FS cells connected only by electrical synapses. Step-coupling coefficient = 2.6%. Spike-coupling coefficient = 0.60%. (B) Isolated spikes were generated with near-threshold presynaptic injections. Spontaneous action potentials were aligned and averaged. Traces are the average of 17 trials. (3-month- and 2-week-old mouse). (C) Single traces showing spikelets transmitted in response to a discharge of presynaptic action potentials. Step-coupling coefficient = 3.7%. Spike, coupling coefficient = 0.94% (11-week-old mouse). (D) Brief trains of presynaptic action potentials result in a transient postsynaptic hyperpolarization. Single traces, data from A, B, and D are from same pair of cells.

Fig 4.

Fig 4.

Paired recording from two PV-FS cells (3 months and 2 weeks old) connected by both electrical and chemical synapses. IPSPs were recorded keeping the postsynaptic neuron under current-clamp at two different potentials (−51 and −92 mV). IPSC was recorded holding the postsynaptic neuron under voltage-clamp at −50 mV. Traces are the average of 50 trials. Step-coupling coefficient = 1.1%.

Fig 5.

Fig 5.

Bar plot showing the percentage of recorded pairs of PV-FS cells connected by electrical and chemical synapses in adult mice.

Fig 6.

Fig 6.

(A) A pair of PV-FS cells electrically coupled and reciprocally connected through chemical connections. Step-coupling coefficient = 1.8 and 1.9%. Spike-coupling coefficient = 0.32 and 0.40% (2-month-old animal). (B) Histogram summarizing paired-pulse ratios (PPRs) from 24 connections. (C) Plot comparing the amplitude of IPSP2 versus IPSP1 for individual events (R = 0.061). The paired-pulse ratio in this connection was 0.61 (3-month- and 2-week-old animal).

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