Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics

Author:

Koch Nils A.ORCID,Corrigan Benjamin W.,Feyerabend Michael,Gulli Roberto A.,Jimenez-Sosa Michelle S.,Abbass MohamadORCID,Sunstrum Julia K.,Matovic Sara,Roussy Megan,Luna Rogelio,Mestern Samuel A.,Mahmoudian Borna,Vijayraghavan Susheel,Igarashi Hiroyuki,Pradeepan Kartik S.,Assis William J.,Pruszynski J. AndrewORCID,Tripathy ShreejoyORCID,Staiger Jochen F.,Gonzalez-Burgos GuillermoORCID,Neef Andreas,Treue Stefan,Everling Stefan,Inoue Wataru,Khadra AnmarORCID,Martinez-Trujillo Julio C.

Abstract

AbstractRecordings of cortical neurons isolated from brain slices and dissociated from their networks, display intrinsic spike frequency adaptation (I-SFA) to a constant current input. Interestingly, extracellular recordings in behaving subjects also show extrinsic-SFA (E-SFA) in response to sustained visual stimulation. Because neurons are isolated from brain networks in slice recordings, it is challenging to infer how I-SFA contributes to E-SFA in interconnected brains during behavior. To investigate this, we recorded responses of macaque lateral prefrontal cortex neuronsin vivoduring a visually guided saccade task and in acute brain slicesin vitro. Broad spiking (BS) putative pyramidal cells and narrow spiking (NS) putative inhibitory interneurons exhibited E-SFAin vivo. In acute brain slices, both cell types displayed I-SFA though their magnitudes differed. To investigate howin vitroI-SFA contributes toin vivoE-SFA, we developed a data-driven hybrid circuit model in which local NS neurons are driven by BS input. We observed that model NS cell responses show longer SFA than observedin vivo. Introducing inhibition of NS cells to the model circuit removed this discrepancy. Our results indicate that both I-SFA and inhibitory circuit dynamics contribute to E-SFA in LPFC neurons. They highlight the contribution of single neuron and network dependent computations to neural activity underlying behavior.

Publisher

Cold Spring Harbor Laboratory

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