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The Journal of Neuroscience, April 13, 2005, 25(15):3857-3869; doi:10.1523/JNEUROSCI.5027-04.2005

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Behavioral/Systems/Cognitive
Feedforward Inhibition of Projection Neurons by Fast-Spiking GABA Interneurons in the Rat Striatum In Vivo

Nicolas Mallet,¹ Catherine Le Moine,¹ Stéphane Charpier,² and François Gonon¹

¹Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5541, Université Victor Segalen Bordeaux 2, 33076 Bordeaux, France, and ²Institut National de la Santé et de la Recherche Médicale, Unité 114, Chaire de Neuropharmacologie, Collège de France, 75231 Paris, France

Discharge activities and local field potentials were recorded in the orofacial motor cortex and in the corresponding rostrolateral striatum of urethane-anesthetized rats. Striatal projection neurons were identified by antidromic activation and fast-spiking GABAergic interneurons (FSIs) by their unique characteristics: briefer spike and burst responses. Juxtacellular injection of neurobiotin combined with parvalbumin immunohistochemistry validated this identification. Spontaneous activities and spike responses to cortical stimulation were recorded during both states of cortical activity: slow waves and desynchronization. Both FSI and projection neurons spontaneously discharged synchronously with slow waves at the maximum of cortical activity, but, on average, FSIs were much more active. Cortical desynchronization enhanced FSI activity and facilitated their spike responses to cortical stimulation, whereas opposite effects were observed regarding projection neurons. Experimental conditions favoring FSI discharge were always associated with a decrease in the firing activity of projection neurons. Spike responses to cortical stimulation occurred earlier (latency difference, 4.6 ms) and with a lower stimulation current for FSIs than for projection neurons. Moreover, blocking GABA_A receptors by local picrotoxin injection enhanced the spike response of projection neurons, and this increase was larger in experimental conditions favoring FSI responses. Therefore, on average, FSIs exert in vivo a powerful feedforward inhibition on projection neurons. However, a few projection neurons were actually more sensitive to cortical stimulation than FSIs. Moreover, picrotoxin, which revealed FSI inhibition, preferentially affected projection neurons exhibiting the weakest sensitivity to cortical stimulation. Thus, feedforward inhibition by FSIs filters cortical information effectively transmitted by striatal projection neurons.

Key words: basal ganglia; striatum; GABAergic; interneuron; parvalbumin; spiny neuron

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Received Sep 30, 2004; revised February 22, 2005; accepted March 1, 2005.

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