Laminar Population Analysis: Estimating Firing Rates and Evoked Synaptic Activity From Multielectrode Recordings in Rat Barrel Cortex

Abstract

Einevoll GT, Pettersen KH, Devor A, Ulbert I, Halgren E, Dale AM. Laminar population analysis: estimating firing rates and evoked synaptic activity from multielectrode recordings in rat barrel cortex. J Neurophysiol 97: 2174 -2190, 2007. First published December 20, 2006; doi:10.1152/jn.00845.2006. We present a new method, laminar population analysis (LPA), for analysis of laminar-electrode (linear multielectrode) data, where physiological constraints are explicitly incorporated in the mathematical model: the high-frequency band [multiunit activity (MUA)] is modeled as a sum over contributions from firing activity of multiple cortical populations, whereas the low-frequency band [local field potential (LFP)] is assumed to reflect the dendritic currents caused by synaptic inputs evoked by this firing. The method is applied to stimulus-averaged laminar-electrode data from barrel cortex of anesthetized rat after single whisker flicks. Two sample data sets, distinguished by stimulus paradigm, type of applied anesthesia, and electrical boundary conditions, are studied in detail. These data sets are well accounted for by a model with four cortical populations: one supragranular, one granular, and two infragranular populations. Population current source densities (CSDs; the CSD signatures after firing in a particular population) provided by LPA are further used to estimate the synaptic connection pattern between the various populations using a new LFP template-fitting technique, where LFP population templates are found by the electrostatic forward solution based on results from compartmental modeling of morphologically reconstructed neurons. Our analysis confirms previous experimental findings regarding the synaptic connections from neurons in the granular layer onto neurons in the supragranular layers and provides predictions about other synaptic connections. Furthermore, the time dependence of the stimulus-evoked population firing activity is predicted, and the temporal ordering of response onset is found to be compatible with earlier findings. I N T R O D U C T I O NExtracellular recordings using multielectrode arrays are uniquely suited to bridge the gap between classical single-cell electrophysiology and noninvasive extracranial EEG/MEG recordings. However, the relationship between extracellular field potentials and population firing rates, and the behavior of specific neuronal cell types and circuits, is poorly understood. In this paper we describe a novel framework for estimation of spiking and synaptic activity in identified cortical neuronal populations, based on laminar array recordings. This approach also provides a means to constrain and validate computational models of neuronal cortical circuits (Dayan and Abbott 2001; Koch and Segev 1998).Technology for large-scale electrical recording of neural activity is rapidly improving, enabling routine measurement of electric potentials from large numbers of closely spaced locations (Buzsaki 2004;Nadasdy et al. 1998). Local field potentials (LFP), i.e., the low-fre...

Comprehensive mapping of whisker-evoked responses reveals broad, sharply tuned thalamocortical input to layer 4 of barrel cortex

“…1D; see METHODS). As shown previously (Di et al 1990;Castro-Alamancos and Oldford 2002;Einevoll et al 2007;Higley and Contreras 2007;Quairiaux et al 2007), the response to the PW deflection was characterized by a sink with the shortest latency to onset (5.0 ms, indicated by small square) and to peak (7.4 ms) in the two electrodes corresponding to granular L4 (Fig. 1D, green rectangle).…”

Suppressed Neuronal Activity and Concurrent Arteriolar Vasoconstriction May Explain Negative Blood Oxygenation Level-Dependent Signal

“…MUA and LFP were recorded using two linear (depth) electrode arrays (Pettersen et al, 2006;Einevoll et al, 2007). The first array was inserted at the center of the active area.…”

“…Given a large point spread function of LFP, this signal is likely to represent a "pick up" of the response in the center rather than local activity in the surround ( (Pettersen et al, 2006) (for review, see Logothetis, 2002). It should be noted that VSD and LFP measure different aspects of neuronal activity in that VSD reflects mean membrane polarization, strongly weighted toward superficial cortical layers, whereas LFP are determined by the spatial distribution of transmembrane currents in a volume around the electrodes (Nicholson and Freeman, 1975;Pettersen et al, 2006;Einevoll et al, 2007).…”

Tuned solutions in dynamic neural fields as building blocks for extended EEG models

“…Such models might render higherdimensional adaptations to the standard equations in EEG models necessary. This can include generators in different laminae and with different spectral properties as they have been reported in experiments (see, e.g., Einevoll et al 2006;Buzsaki 2004 and references therein). Following the way outlined here, the gap between coarse-grained EEG models and more local models for cortical tuning may be bridged one step further.…”