Interaction between afferent excitation and feed-forward inhibitionin the recruitment of hippocampal neuronal ensembles.

FREDERIC POIULLE; ANTONIA MARIN BURGIN; MASSIMO SCANZIANI

San Diego

Congreso; Meeting of the society for neuroscience; 2007

Society for Neuroscience

The identity of neurons active within a network reflects structural and temporal features of its afferent inputs. Here we investigate the synaptic mechanisms leading to the recruitment of specific ensembles of hippocampal CA1 pyramidal cells (PCs) in response to the activity of their main excitatory afferents, the Schaffer collaterals (SCs).In acute hippocampal slices from 3-4 weeks old rats, small regions of the CA1 PC layer were loaded with the calcium indicator dye OGB-AM in order to detect action potential evoked calcium transients in PC somata.Stimulation of SCs with an electrode placed in the stratum radiatum resulted in the recruitment of a fraction of the loaded PC population, as detected by the relative change in fluorescence; this fraction increased with stimulation intensity. Stimulation of two independent SC pathways resulted in the recruitment of two different PC ensembles. The number of PCs shared by the two ensembles was directly proportional to the fraction of the PC population activated by each of the two SC pathways.By recruiting local GABAergic interneurons SCs also inhibit PCs in a feed-forward manner. Accordingly, perfusion of the GABAA receptor antagonist gabazine increased the fraction of PCs recruited by SC stimulation. These results indicate that the specific ensemble of PCs recruited in response to SC stimulation results from the interaction between excitatory and inhibitory inputs onto each PC.What determines the specific ensembles recruited by SC stimulation? We can hypothesize two extreme scenarios: 1) All PCs in the population receive a similar amount of excitation, but different amounts of inhibition; in this case, the PCs belonging to the recruited ensemble are those that receive less inhibition. 2) All PCs in the population receive a similar amount of inhibition, but different amounts of excitation; therefore, the PCs belonging to the recruited ensemble are those that receive more excitation.To discriminate between these two possibilities, we stimulated the SCs to recruit an ensemble of PCs and performed simultaneous whole-cell voltage-clamp recordings from two neighboring PCs; one PC belonged to the recruited ensemble, the other not. While disynaptic feed-forward inhibition was the same in the two PCs, monosynaptic excitation was on average twice as large in the PC belonging to the recruited ensemble.These results indicate that while feed-forward inhibition homogenously affects the entire PC population, monosynaptic excitation specifically parses the population into different ensembles.